Proc. Nat. Acad. Sci. USAVol. 73, No. 4, pp. 1360-1364, April 1976Zoology

Rates, patterns, and effectiveness of evolution in multi-levelsituations

(speciation/adaptation/feedback/numbers effects/human evolution)

P. J. DARLINGTON, JR.Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts 02138

Contributed by P. J. Darlington, Jr., December 15, 1975

ABSTRACT Evolution is a multi-level process. Both actu-al evidence and theoretical considerations suggest as a firstgeneralization that evolution both at single levels and in se-ries of increasingly complex levels decelerates with time. Ad-ditional evidence, the expected difference between rapidnonadaptive speciation in small populations and effectiveadaptation in large ones, and analysis of explosive evolutionsuggest further that effective adaptive evolution occurs pri-marily in large populations, and that segments of such evolu-tion tend to begin slowly; accelerate, sometimes explosively,and then decelerate. The segments are irregular, and do notoccur at regular intervals. However, the explosive evolutionof a generaI adaptation pre-adapts to and is often followedby an explosive radiation of derivative lineages. This descrip-tion seems to fit the origin and initial radiation of mammaIs,and the evolutionary history of man and man's cultures.

Evolutionists recognize that evolution is a multi-level processbut rarely apply the multi-level concept consistently. Here, Ishall try to apply it to an analysis of rates, patterns, and ef-fectiveness of evolution, which is a subject of current inter-est. For a statement of some of the concepts of multi-levelevolution see ref. 1.

FACTS AND PROBABILITIESThe "Law" of Acceleration. Bernal (ref. 2, pp. 107-109),

following Oparin and others, refers to ". . . the general lawof the acceleration of the evolutionary process with time,"and gives as an example a supposed "speeding up" of evolu-tion during the evolutionary sequence of land animals,mammals, primates, man, and man's cultures through thestone, bronze, and iron ages and the age of science. How-ever, although primates originated more recently and haveexisted for a shorter time than mammals, and mammals than"land animals," it does not follow that the more recentgroups have evolved more rapidly. The question that shouldbe asked is, have primates evolved more rapidly than thefirst land vertebrates or the first mammals did in compara-ble time spans? And the answer is, we do not know.

Nevertheless, two facts remain which seem at firstthought to be consistent with Bernal's generalization. One isthe unquestioned acceleration of evolution of human cul-tures. The other is the longer time of existence of simpler,prokaryote organisms compared with the shorter time of ori-gin and diversification of higher, more complex eukaryotes.This second fact needs critical examination.

Prokaryote and Eukaryote Histories. Prokaryotes (rela-tively simple precellular and unicellular organisms withoutdistinct nuclei) existed for a very long time, apparently morethan 2 billion years, before the appearance of eukaryotes,but their evolution need not have been uniformly slow. Thefossil evidence, what little there is of it (well summarized inref. 3, pp. 601ff; see also ref. 4), indicates that both bacteriaand blue-green algae existed at least 3.1 billion years ago

and may already have been using chlorophyll, and thissuggests that the main groups of prokaryotes evolved andseparated rapidly, very early in their history, and that evolu-tion of their primary adaptations then slowed down ratherthan speeded up.

Supposed fossil eukaryote cells in the Bitter Springs for-mation in the Late Precambrian of Australia are nowthought to be partially degraded prokaryote blue-greenalgae, and all other older supposed eukaryote fossils aredoubtful too, according to a very recent paper by Knoll andBarghoorn (5). These authors think that the eukaryote (nu-cleated) cell may not have originated until just before theCambrian, less than 1 billion years ago, and that multicellu-lar eukaryotes may then have evolved "quite rapidly"; allthe major eukaryote phyla, except the chordates, appear fos-sil in the Cambrian. This suggests a period of rapid evolutionand primary adaptive radiation of eukaryotes, followed by aslowing down of the primary lines of adaptation. (But theunknown earlier stages of evolution of the exceedingly com-plex eukaryote cell may have been more gradual.)

So, it is an hypothesis consistent with the apparent factsthat prokaryote and eukaryote origins followed a commonpattern, of a period of rapid evolution and diversification,followed by a slowing down of the primary adaptive pro-cesses, although in both cases secondary adaptive radiationsoccurred from time to time in separate phyletic lines.

Fossil Evidence of Rates of Evolution. Simpson (6) de-scribes actual rates of evolution indicated by the fossil rec-ord. He concludes that the rates have varied enormously indifferent comparable groups at the same time, and in thesame groups at different times, and (ref. 6, p. 139) that mostof what we now think of as slow-rate lines of evolution prob-ably went through periods of rapid evolution in the past, andhave decelerated.

These considerations, facts, and probabilities raise seriousdoubts about the validity of the "general law" of accelera-tion of evolution as stated and exemplified by Bernal, andsuggest a different generalization: that distinguishable seg-ments of adaptive evolution tend to be rapid for a time andthen decelerate. [The term "segment" is suggested for anyportion of an evolutionary continuum which has a distin-guishable history. The term includes, but is broader than,Simpson's (ref. 6, pp. 206-217) "quantum" of evolution.]

THEORETICAL CONSIDERATIONSComparisons, Measurements, and Factors. Comparisons

of evolutionary rates at different levels are difficult. Howare rates of evolution of, say, hypothetical original livingmolecules or existing viruses, prokaryote blue-green algaewhich do not reproduce sexually, and sexually bonded popu-lations of higher plants or animals to be measured and com-

1360

Dow

nloa

ded

by g

uest

on

Mar

ch 3

0, 2

020

Proc. Nat. Acad. Sci. USA 73 (1976) 1361

pared? Time of speciation cannot well be taken as a mea-sure, for "species" are not comparable in the different cases.Perhaps comparisons should be made at molecular levels inall cases. Then the question becomes, how do rates of molec-ular evolution compare at different levels? Or, if existinggenes are comparable to early living molecules, how do theirrates of evolution compare? This question can hardly be an-swered now.Something can be said, however, about a possible relation

between complexity and evolutionary rates. Other thingsbeing equal, directional changes might be expected to occurmore rapidly in simple sets (in relatively simple molecules,simple organisms [simple sets of genes], and simple groups oforganisms) than in more-complex ones. If so, evolution ofprotobionts and the first living molecules may have been rel-atively rapid, and rates of evolution may have decreased asorganisms increased in complexity, reversing the "law" ofthe acceleration of evolution with time. Whether this actual-ly happened is another question which can hardly be an-swered now.A relation presumably exists also between position in an

adaptive segment of evolution, the force of selection, andthe rate of evolution. When an organism has begun to make(evolve) an advantageous adaptation but is far from havingmade it, the force of selection is presumably strong at firstand decreases as the organism approaches a fully adaptedstate, and the rate of evolution should therefore be rapid atfirst and should decelerate.

Therefore, for the two reasons given (that changes wouldbe expected to occur more rapidly in simple than in complexsets, and that in segments of adaptive evolution selectiveforces would be expected to be strong at first and to weakenas fully adapted states are approached), the law (if there is alaw) might be expected to be that evolution at any level, andin series of increasingly complex levels, decelerates withtime. Some notable segments of evolution seem to have hadthis history.

This generalization is plainly too simple, at best half true.It is further considered under Explosive Evolution below.First, however, some modifying and complicating factorsare to be considered.

Small versus Large Populations. Several recent writers(e.g., refs. 7 and 8) think that speciation occurs most rapidlyin small peripheral populations, and that major changes inevolving lineages occur by "speciation events" (rapid evolu-tions and selective extinctions of many small-populationspecies) rather than by continuing change in large popula-tions. (These writers call the latter process "phyletic gradual-ism," but this is a prejudicial phrase.) Within the limits ofthis short paper, these alternatives can be compared only bymeans of briefly stated propositions.

Proposition 1: Hypotheses Compatible. Harper (9)seems to assert, or perhaps he intends to quote (7), that thehypotheses of small- and large-population evolution cannotboth be true. However, small- and large-population speciesoften coexist in the same lineages. They probably havesomewhat different modes of evolution, but their evolutionsseem to me to be compatible and probably complexly inter-related, as suggested in Proposition 10. (And Harpersuggests intermediate models.)

Proposition 2: Fossil Evidence Ambiguous. Fossils showthe course of evolution but not its mode during (for exam-ple) the origin and radiation of mammals or the rapid Pleis-tocene evolution of man. Eldridge and Gould (7), in their

small-population evolution, do not give the potentialities oflarge-population evolution "equal time," but they add (ref.7, p. 99), probably correctly, that "the data of paleontologycannot decide" which kind of evolution has occurred in ac-

tual cases.

Proposition 3: Detectability of Processes. In lineages inwhich both speciation and continuing adaptation have oc-

curred, fossils are likely to show the structural radiations andspeciations more clearly than the adaptive processes. For ex-

ample, the structural radiation and speciation of mammalsat the beginning of the Tertiary is more clearly shown thanthe evolution of mammalian warm-bloodedness (furtherconsidered in Proposition 9).

Proposition 4: Rate versus Effectiveness; Special versus

General Adaptation. Distinctions should be made betweenthe rate of evolution and its adaptive effectiveness, and be-tween special adaptations (to single environments or singlefactors in the environment) and general adaptations (whichincrease fitness in many environments and pre-adapt toadaptive radiations) (ref. 10). Small-population evolution is arelatively random process. It may be rapid and may producelimited special adaptations, but it is unlikely to producemore-complex general adaptations. Large-population evolu-tion, on the other hand, varies enormously in rate but can berapid under appropriate conditions; it is less random andmore likely to be effective in producing complex general ad-aptations.

Proposition 5: Potentialities of Large Populations. Mod-em Darwinians take as a tenet, originally promulgated byWright but now so widely accepted that references are un-

necessary, that a large population divided into many demes(as many large populations are), which exchange individualsonly occasionally, may evolve both rapidly and effectively.For example, a large-population species of ION individuals,divided into 10 demes of IN individuals, may evolve almostas rapidly in one direction as any one of 10 small-populationspecies each of IN individuals. If rapid evolution depends on

breaking of complex evolutionary homeostases, small demescan probably do it effectively enough. The separate IN pop-ulations can diversify (evolve in different directions) more

widely, promoting evolutionary "explorations," but the 10 XIN population can "explore" too, within narrower limits,and has other, overwhelming advantages. It can put togetherselectively advantageous events that occur in differentdemes. If rare mutations, which occur only once in billionsof individuals, are important in evolution (we do not know ifthey are), each is 10 times more likely to occur in the iONthan in a IN population, and if a series of x such mutations isrequired for evolution of a given adaptation, the ION popu-lation may be l0x times more likely than a IN population tocomplete the series in a given time. And when, as is proba-bly often the case, a major (general) adaptation involves theputting together of an almost endless series of mutations andrecombinations (as in the evolution of a behavior outlinedbelow), the advantage of the larger population must, in realcases, be almost incalculably great.

Proposition 6: The Complexity of Adaptation. Generaladaptations, such as warm-bloodedness, involve complex in-teractions of structure, function, physiology, and behavior.Their evolutions must be complex. This is especially true ofthe evolution of an effective new behavior. It probably usu-

ally begins by the doing of something new: by a tentativespreading into a new environment or the adding of a tenta-tive new behavior to a preexisting behavioral repertory. If

forceful and useful presentation of evidence consistent with

Zmcclogy: Darlington

the new behavior is selectively advantageous, all its compo-

Dow

nloa

ded

by g

uest

on

Mar

ch 3

0, 2

020

Proc. Nat. Acad. Sci. USA 73 (1976)

nents evolve. The skeleton may evolve, and this is usually allthat will show in the fossil record. But correlated evolution-ary changes must often occur also in muscles, blood supply,metabolism, endocrine systems, nerve circuits, and thebrain's cortex. Each of these changes is likely to require a se-ries of mutations and recombinations on which selectionacts, and some of the subprocesses may require evolution notonly of direct responses but also of feedback controls. Andeven this is not the end of the complexity. The selective ad-vantage of a behavior may depend also on how much the be-havior is used and this may be determined complexly too,partly by evolution of reinforcing sensations of pleasure inthe brain's limbic system (11).

All this is intended to emphasize two points: that paleon-tologists and mathematical evolutionists can see and quanti-ty relatively simple speciation events more easily than theevolution of more complex general adaptations, and thatgeneral adaptations are likely to be almost inconceivablycomplex.

Proposition 7: The Cost of Adaptation. The cost of adap-tation, which is the cost of selection calculated in numbers ofindividuals selectively eliminated or in "genetic deaths," is acomplicated subject, often mishandled by mathematicians,and not yet fully understood. For a recent discussion of it,with references, see ref. 12. The following generalizationsand inferences are pertinent here.

Large populations, with large numbers of surplus individ-uals in each generation, can pay higher costs of adaptationthan small populations can. When a large population paysheavy costs, by selective elimination of many individuals,the population may be reduced in size. It may become tem-porarily a small population. But it does not then have thecharacteristics of a permanently small peripheral popula-tion. It may lose some genes, but it will retain most of theadaptive advantages gained as a large population, and theseadvantages will favor rapid recovery of the population.

Large populations therefore have a double advantage inadaptive evolution: they can put together selectively advan-tageous events that occur separately, and they can pay rela-tively heavy, complex costs of adaptation.

Proposition 8: Numbers Effects, Inter-Level Compro-mises, and Feedbacks. The multi-level concept of evolutionsuggests, as a generalization, that, at every level, largegroups evolve more effectively than small ones at the samelevel. This generalization probably holds at genic levels:large genotypes, or sets of many genes, probably make com-plex adaptations more effectively, if not more rapidly, thansmall ones, or sets of fewer genes; this may be one reasonwhy it is selectively advantageous for organisms to carrynumbers of temporarily unused (neutral and duplicate)genes. It probably holds at cellular levels: multicellular or-ganisms of many cells can probably make complex adapta-tions more effectively, if not more rapidly, than can those offewer cells. It probably holds-this is stressed in the presentpaper-at the level of populations: large populations, ofmany individuals, probably evolve more effectively, if notmore rapidly, than small ones. And it seems to hold also at astill higher level: evolution seems to be most effective wheremany species occur together in large- areas and tropical cli-mates; this seems to be the explanation of the apparent ten-dency of successive dominant groups of animals to evolve inand disperse from large tropical areas (10).Of course numbers effects must be much more complex

than this. There must often be an upper limit to the size

sumably there are numbers optima in many cases. And theremust be interactions and compromises, with feedbacks, be-tween levels. For example, numbers of individuals in popu-

lations and numbers of populations (species) that occur to-gether must be complexly interrelated. These complexitiesdo not impair the theoretical principles, but do make it diffi-cult to detect and evaluate numbers effects in real cases.

Proposition 9: Explosive Evolution. The concept of evo-

lution as a multi-level process of directional change in setsallows comparisons to be made even between the highestlevels of organic evolution and inorganic processes. A ques-

tion that can then be asked is, can "explosive evolution" beusefully compared with simpler explosions?

Simple chemical processes are often self-propagating andself-accelerating. For example, a hearth fire starts when thetemperature of a small portion of the fuel is raised to thepoint at which oxidation begins, and the fire then propagatesitself by generating the heat it needs to continue. There isalso some self-acceleration at the beginning of most fires,and they become explosive when the distribution of fuel andoxygen results in very rapid self-acceleration. Both numbersor mass effects and feedbacks are involved in this. However,the period of self-acceleration is always limited, and is fol-lowed by deceleration and eventual termination of the ex-

plosion.Explosive organic evolution, as evolutionists including

Simpson (ref. 6, pp. 89, 139, and 213) usually describe it, oc-

curs when, from a common ancestor, many different linea-ges evolve rapidly in different directions, becoming adaptedto different environments or different roles in the environ-ment. As thus described, it is equivalent to rapid adaptiveradiation. However, explosive evolution sometimes seems tobe more than this, to be both self-propagating and some-

times self-accelerating.These characteristics are to be expected even in relatively

simple segments of adaptive evolution. For example, the ev-olution of a Batesian mimic might begin if the potentialmimic at first resembled the model only distantly, and if thedistant resemblance resulted in survival of only an occasion-al individual under unusual circumstances, perhaps only indim light or when an individual mimefactor (predator in-ducing mimicry) was inexperienced. Such a resemblancewould have only a slight selective advantage at first, and itsrate of evolution would be slow. However, as the resem-blance became closer, its selective advantage would presum-ably increase, and its rate of evolution would increase. Its ev-olution would then be both self-propagating and self-accel-erating. But the period of self-acceleration would be limited.As the resemblance became very close, both the possibilityand the advantage of further improvement would decrease,and so would the force of selection and the rate of evolution.The evolution of the mimic would therefore be expectedfirst to accelerate and then to decelerate.The evolution of placental mammals exemplifies a more

complex explosive pattern. The primary general adaptationof primitive mammals was probably warm-bloodedness or,more accurately, a shift from behavioral toward increasinglyphysiological thermoregulation. (This may have permittedand been correlated with evolution of placental reproduc-tion, a better brain, and other general adaptations.) The de-tailed evolutionary changes in this direction were perhapsslight at first and conferred only slight selective advantages,so that they evolved slowly. Division of the palate in someTriassic fossil therapsid reptiles suggests that the ancestors of

(number of members) of effective groups at any level; pre-

1362 Zoology: Darlington

mammals were beginning to become warm-blooded then

Dow

nloa

ded

by g

uest

on

Mar

ch 3

0, 2

020

Proc. Nat. Acad. Sci. USA 73 (1976) 1363

(ref. 13, p. 237). If so, the earlier stages of evolution of mam-malian warm-bloodedness may have proceeded slowly forsomething like a hundred million years, from the Triassic tothe Late Cretaceous; the complexities of the homeostatictemperature controls may well have required a long timespan for their evolution. Then, this segment of evolution ap-

parently accelerated, or at least reached a point at which itconferred great advantages. Perhaps hair, which greatly in-creased the effectiveness of body insulation, evolved then.And then, when the complex physiological processes con-

cerned approached effective-limits, the force of selection de-creased and the rate of evolution of the primary adaptationpresumably decelerated. However, the general selective ad-vantage conferred at the climax of the primary adaptivesegment of evolution was so great that the animals con-

cerned-Late Cretaceous and early Tertiary placental mam-mals-radiated explosively in secondary ways.

Proposition 10: Generalization. In more general terms,an evolutionary explosion probably begins as an adaptiveprocess which (like simpler explosions) is self-propagating,with numbers effects and feedbacks. It does or may beginslowly, accelerate, and then decelerate. But if the primaryadaptation is a general one conferring a great selective ad-vantage, it may be followed by an explosive radiation in-volving secondary adaptations and conspicuous speciations.These two parts of evolutionary explosions-the primary ad-aptations and the secondary radiations-should be clearlydistinguished. The first part is probably mainly a large-pop-ulation process; only large populations can encompass thecomplexities and pay the costs of complex adaptation. Thesecond part may be more a small-population, "speciationevent" process, in which a partial shift occurs from adapta-tion (which continues) to increasing randomness; this process

may be rapid but is of less long-term significance than theother.

These two processes are probably complexly interrelated.Evolution of a very advantageous general adaptation is like-ly to be followed by a very extensive secondary adaptive ra-

diation and multiplication of species; and the diversity ofspecies, each possessing the advantages of the general adap-tation plus its own special adaptations and random geneticeffects, should increase the chance of a break-through into a

new adaptive zone and the beginning of a new segment ofgeneral adaptation.

If all this is correct, evolutionary explosions and rates ofevolution in general are, if not cyclical, at least segmental,each well-defined segment of adaptive evolution tending to

have a history of acceleration and deceleration, sometimesfollowed by conspicuous secondary adaptive radiation andspeciation. The segments are irregular, and they do not

occur at regular intervals, but they do tend to form irregularsequences of primary, secondary, tertiary, etc. adaptationsand radiations. This is presumably the pattern of evolutionat all levels at which adaptation occurs. And events at differ-ent levels interact, with numbers effects and feedbacks. Thecomplexity of the whole is inconceivable-literally beyondthe power of the human brain to conceive of-but the prin-

ciples are real and well worth attempting to apply to (for ex-

ample) the evolution of man and of human cultures.

APPLICATION TO MAN

The evolution of man can be dealt. with here only by a seriesof additional propositions.

tion of ape into man began with evolution of an erect pos-ture and bipedal locomotion. Of this segment of physical ev-olution fossils show only that australopithecines suitable tobe man's ancestors stood nearly erect at least 5 million yearsago, but it is a reasonable inference that evolution of erectposture and two-legged running had accelerated understrong selective pressure when prehumans first moved intoopen country, and then decelerated.The second segment of man's physical evolution was an

increase in size of brain. Fossils indicate that the increasewas slow in the australopithecines, accelerated during the di-vergence and evolution of Homo, then decelerated, and vir-tually stopped several tens of thousands of years ago. (Somecomplexities in this oversimplified history are suggested byref. 14.)

Proposition 12: Evolution of Brain Capability. A consis-tent but unprovable hypothesis is that evolution of brain ca-pability was closely correlated with evolution of brain size;that after rapid evolution of an erect posture had freed thearms and hands for new functions, throwing (of stones andweapons) induced gradual evolution of an increasingly com-plex and precise brain in australopithecines (11); that thispre-adapted the brain to evolve still more complex and pre-cise capabilities including ability to communicate by lan-guage, and that the selective advantage of the latter inducedan acceleration of brain evolution in Homo; and that whenbrain evolution approached effective limits (or was limitedby other factors), the evolution of both brain size and braincapability decelerated.

Proposition 13: Secondary Evolutions. Evolution in.Homo of a brain with increasingly complex and precisecapabilities initiated secondary evolutions of increasinglycomplex behaviors, social organizations, cultures, technolo-gies, and philosophies. These had no independent existencebut were all manifestations of evolutions of sets of interact-ing bits of living material in single brains and sets of inter-acting brains. The evolution of some behaviors included ge-netically determined changes in "innate" components, butmost of the secondary evolutions involved social rather thangenetic heredity, variation, and selection. [From a multi-level point of view, the shift from genetic to social hereditydid not end competition and natural selection (= differentialelimination) but shifted them to a new level where they aremore difficult to quantify but perhaps more amenable to in-telligent control.] The secondary evolutions began while thebrain itself was still evolving, continued after brain evolutionhad decelerated, and are accelerating explosively now.The secondary evolutions varied in their adaptive preci-

sion. Evolving man apparently needed and perhaps stillneeds religions, mystic cults, and philosophies. These pre-sumably conferred a common selective, adaptive advantage,but precise differences among them seem to have been rela-tively nonadaptive; to paraphrase Kim's Mahbub Ali, allfaiths have had merit in their own demes. They may haveevolved and diversified by a process comparable to nonad-aptive speciation in small populations. The evolutions of cul-tures have been too complex to consider here. But technolo-gies are relatively simple and precise, and do seem to haveevolved both rapidly and effectively in large, deme-dividedpopulations of brains. This cannot be argued in detail here.Readers may, if they wish, work out for themselves whethersegments of technological evolution, such as the evolution ofagriculture or of atomic technology, have evolved most ef-fectively in large populations of brains, divided into demesthat have exchanged technological details occasionally, with

Zoology: Darlington

Proposition I 1: Physical Evolution of Man. The transi-

Dow

nloa

ded

by g

uest

on

Mar

ch 3

0, 2

020

Proc. Nat. Acad. Sct. USA 73 (1976)

self-propagation and self-acceleration, numbers effects, andfeedbacks.

Proposition 14: Man a Large-Population Species. Manhas been a large-population species, divided into manydemes, at least since subpopulations reached Australia andAmerica twenty or thirty thousand or more years ago. Anhypothesis consistent with this fact is that one ancestral pop-ulation of Australopithecus, divided into many demes, oc-cupied much of Africa and southern Asia-fossil fragmentsindicate that australopithecines did range this widely, butcannot show whether they were demes of one species; thatsince then man's ancestors have maintained a large, deme-divided population of the sort theoretically capable of effec-tive as well as rapid adaptive evolution; and that man's dis-tinctive physical characteristics, brain capability, and com-plex behaviors and cultures have evolved and are evolving insuch a population.

Proposition 15: Final Statement. The evolution of manhas included primary adaptive segments during which evo-lution has first accelerated and then decelerated, followedby an explosive secondary radiation of behaviors, cultures,etc. It is comparable to the evolution of other general adap-tations followed by secondary radiations, and is the best ex-ample we have-closest to us and most accessible for analy-sis-of this multi-level evolutionary pattern.

Almost every statement of fact and every generalizationin this short paper has, of necessity, been oversimplified.The paper is, in fact, "verbal theorizing" of a sort sometimesbelittled by experimental and mathematical biologists andothers preoccupied with details. However, 1 think it is essen-tial that what might be called the "detail explosion" in biol-ogy-the self-accelerating, exponential, explosive increase ofknowledge of details of life at all levels-be balanced by for-mulation of simple principles by which the details can be or-ganized and understood, and by which organic evolutioncan be related to other processes of directional change. Thatsuch principles can be formulated ought to be the first tenetof multi-level evolution theory.The following reference list cannot be exhaustive, but

should serve as an introduction to the literature on rates and

modes of evolution. Simpson (6) is still essential reading onthis subject, and Frazzetta (12) is a good recent discussion ofsome aspects of it. And see ref. 15 for the possible roles ofgene-regulator systems in permitting rapid evolution, and ofcontinental drift in timing evolutionary episodes. (I suggestthat gene-regulators are more effective in secondary diversi-fications than in primary evolutions of new genetic-struc-tural-functional systems, and that, while continental driftmay make opportunities for special adaptations, it cannot berelated to the more fundamental, more complex, and morenovel general adaptations that seem often to have precededmajor diversifications, for example in evolution of the eukar-yote cell, of mammalian warm-bloodedness and placentalreproduction, and of the human brain.)1. Darlington, P. J., Jr. (1972) Proc. Nat. Acad. Scd. USA 69,

1239-1243.2. Bernal, J. D. (1967) The Origin of Life (Weidenfeld and Ni-

colson, London).3. Wilson, E. O., Eisner, T., Briggs, W. R., Dickerson, R. E.,

Metzenberg, R. L., O'Brien, R. D., Susman, M. & Boggs, W.E. (1973) Life on Earth [Sinauer Associates, Stamford, Conn.(now Sunderland, Mass.)].

4. Cloud, P., Moorman, M. & Pierce, D. (1975) Q. Rev. Biol. 50,131-150.

5. Knoll, A. H. & Barghoorn, E. S. (1975) Science 190,52-54.6. Simpson, G. G. (1965, reprinted from 1944) Tempo and Mode

in Evolution (Hafner Publishing Co., New York).7. Eldredge, N. & Gould, S. J. (1972) in Models in Paleobiology,

ed. Schopf, T. J. M. (Freeman, Cooper & Co., San Francisco,Calif.), pp. 82-115.

8. Stanley, S. M. (1975) Proc. Nat. Acad. Sci. USA 72,646-650.9. Harper, C. W., Jr. (1975) Science 190, 47-48.

10. Darlington, P. J., Jr. (1959) Evolution 13,488-510.11. Darlington, P. J., Jr. (1975) Proc. Nat. Acad. Sci. USA 72,

3748-3752.12. Frazzetta, T. H. (1975) Complex Adaptations in Evolving

Populations (Sinauer Associates, Sunderland, Mass.).13. Romer, A. S. (1968) The Procession of Life (Weidenfeld and

Nicolson, London).14. McHenry, H. M. (1975) Science 190,425-431.15. Valentine, J. W. & Campbell, C. A. (1975) Am. Sci. 63, 673-

680.

1364 Zoology: Darlington

Dow

nloa

ded

by g

uest

on

Mar

ch 3

0, 2

020