towards a new evolutionary synthesis

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TREE vol. 15, no. 1 January 2000 0169-5347/00/$ see front matter 2000 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(99)01743-7 27

Darwins theory of evolution wasbased on the primarily uniformitar-ian concept that the processes of geneticvariation and natural selection, studiedin modern populations, are sufficient toexplain the large-scale patterns of diver-sification that have occurred throughoutthe billions of years of life on earth. Thepersistence of this viewpoint is evident inrecent editions of numerous universitytextbooks, three of which were reviewedby Moore1. Moore specifically cited the

uniformitarian approach of Ridley inbridging the gap between populationlevel phenomena and larger scale patternsin the history of life. Large-scale phenom-ena continue to be treated in a primarilyhistorical manner, with little consider-ation for the forces that are responsiblefor the origin and long-term perpetuationof basic body plans, major changes instructures and ways of life, or the influenceof abiological factors on critical events inthe history of life. The focus of these text-books, and the majority of papers pub-lished in the journal Evolution, on mod-ern species belies the great advances inother areas of science that contribute tothe understanding of large-scale, long-termevolutionary phenomena.

Research in many disciplines over thepast 40 years has demonstrated that thepatterns, processes and forces of evolu-tion are far more diverse than hypothe-sized by Darwin2 and the framers of theevolutionary synthesis3: (1) Increasingknowledge of the fossil record and thecapacity for accurate geological datingdemonstrate that large-scale patterns

and rates of evolution are not compa-rable with those hypothesized by Darwinon the basis of extrapolation from modernpopulations and species4. (2) Knowledgeof plate tectonics indicates that changesin the position and configuration of the

continents, and their influence on climateand the capacity for dispersal have beenmajor forces in driving evolutionarychange5. (3) The elaboration of phyloge-netic systematics has provided a spe-cifically evolutionary methodology forestablishing relationships6. (4) The mostspectacular contributions have come fromthe field of molecular developmentalbiology, making it possible to understandthe specific manner in which majorchanges in the anatomy and physiology

of organisms have occurred, and how suchchanges can be influenced by naturalselection7.

It is now necessary to incorporatethis rapidly increasing body of informationinto an expanded evolutionary synthesis.

Empirical evidence from thefossil recordThe most obvious contrasts between thedarwinian view of the patterns and therates of evolution, and the evidence thathas since been documented by the fossilrecord, are illustrated in Fig. 1. Darwinused the only illustration in the first editionof The Origin of Species to explain hishypothesis that the patterns of evolutionover hundreds of millions of generationswere the same as those at the level ofpopulations and species. In fact, they areclearly distinct in all taxonomic groups4,8.Evolution at the level of populations andspecies might, in some cases, appear asnearly continuous change accompanied bydivergence to occupy much of the avail-able morphospace9. However, this is cer-tainly not true for long-term, large-scale

evolution, such as that of the metazoanphyla, which include most of the taxathat formed the basis for the evolution-ary synthesis. The most striking featuresof large-scale evolution are the extremelyrapid divergence of lineages near the

time of their origin, followed by long peri-ods in which basic body plans and waysof life are retained. What is missing are themany intermediate forms hypothesizedby Darwin, and the continual divergenceof major lineages into the morphospacebetween distinct adaptive types.

The most conspicuous event in meta-zoan evolution was the dramatic origin ofmajor new structures and body plans doc-umented by the Cambrian explosion10,11.Until 530 million years ago, multicellularanimals consisted primarily of simple,soft-bodied forms, most of which havebeen identified from the fossil record ascnidarians and sponges. Then, within lessthen 10 million years, almost all of theadvanced phyla appeared, includingechinoderms, chordates, annelids, bra-chiopods, molluscs and a host of arthro-pods. The extreme speed of anatomicalchange and adaptive radiation during thisbrief time period requires explanationsthat go beyond those proposed for the evo-lution of species within the modern biota.

Evolution and developmentMost of the history of life, from 3.5 to0.6 billion years ago, was dominated byextremely slowly evolving unicellularorganisms12,13. Their potential for in-creasing complexity was restricted bythe small size of the genome and the lim-ited capacity for genetic recombination.

The low concentration of atmosphericoxygen constrained their size and pre-cluded the formation of supporting skele-tons. Aggregation of identical cells waspossible, but the development of organ-isms with complex body plans composedof many kinds of cells was not possible.Within these constraints, the most signif-icant evolutionary events to occur in themid-Proterozoic (approximately 1.5 bil-lion years ago) were the endosymbiosisbetween species of the Archaea and theEubacteria, which led to the origin of themitochondria and the chloroplasts ofeukaryotes14. These were unique events,only vaguely comparable with otheraspects of the horizontal transfer ofgenetic material that can be studied inliving species15.

Beginning approximately 600 millionyears ago, larger, soft-bodied animalsappeared in the fossil record, includingspecies resembling sponges and cnidari-ans, as well as trails and burrows formedby bilaterally symmetrical, worm-likeforms with a unidirectional digestivetrack. Then, between 530 and 525 million

years ago, all more advanced metazoanphyla appeared and the most rapidlyradiating group, the arthropods, quicklyreached a level of diversity approachingthat of their modern marine descen-dants16. This explosive evolution of phyla

PERSPECTIVES

Towards a new evolutionary synthesis

Robert L. Carroll

New concepts and information from molecular developmental biology, systematics,geology and the fossil record of all groups of organisms, need to be integrated into an

expanded evolutionary synthesis. These fields of study show that large-scale evolutionary

phenomena cannot be understood solely on the basis of extrapolation from processes

observed at the level of modern populations and species. Patterns and rates of evolution

are much more varied than had been conceived by Darwin or the evolutionary synthesis,

and physical factors of the earths history have had a significant, but extremely varied,

impact on the evolution of life.

Robert Carroll is at the Dept of Biology and is Curator of Vertebrate Paleontology, Redpath Museum,

McGill University, 859 Sherbrooke St. West, Montreal, PQ, Canada H3A 2K6

([email protected]).


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28 TREE vol. 15, no. 1 January 2000

with diverse body plans is certainly notexplicable by extrapolation from the pro-cesses and rates of evolution observed inmodern species, but requires a successionof unique events.

The development of complex bodyplans, with many distinct cell types andanatomical structures, required a newsystem of genetic control that is not pre-sent in unicellular organisms. This isbased on a distinct genetic category, theHox gene1720. Hox genes are unique tometazoans but evolved from a more in-clusive group, the homeobox genes,which are also recognized in unicellulareukaryotes and land plants. Homeoboxgenes code for specific proteins that acti-vate other genes, and thus they regulatea host of processes within the cell. Hoxgenes are uniquely arranged in a linearsequence along the chromosome, whichcorresponds with both the linear and thetemporal sequence of their activationalong the anterioposterior axis of theembryo. (MADS-box genes have a compa-

rable role in controlling the position ofmajor structures in land plants21.)The number ofHoxgenes, arranged in

a cluster along a chromosome, is broadlycomparable to the degree of complexityof the organism, with one in sponges, four

to five in cnidarians, six to ten in most ofthe higher metazoan phyla, and up to 39,arrayed in fourHoxclusters on differentchromosomes, in mammals22 (Fig. 2).These genes control the position and theexpression of the major structural fea-tures of the body, including the elementsof the head and the sequence and natureof the appendages.

Although molecular homologies havebeen established forHoxgenes through-out the metazoan phyla, the specific struc-

tures whose position they control can bedifferent, as in the case of the distinctbody forms of the deuterostome phylaChordata and Echinodermata23. This isbecause theHoxgenes act as switches tocontrol the expression of a variety ofgenes, which in turn control differentstructures and cell types.

The origin of multicellularity andcomplex body plans among animals wasa unique phenomenon, dependant on theevolution of Hoxgenes near the end ofthe Precambrian (late Neoproterozoic).

Once evolved, their subsequent dupli-cation and divergent change in adap-tively distinct lineages established thebasis for the radiation of the many meta-zoan phyla24. Most phyla have apparentlyretained a relatively constant number of

Hoxgenes since the Cambrian. A strikingexception is the Chordata, in which thelargest scale change occurred betweenthe cephalochordates and early verte-brates, when the number ofHoxclustersduplicated twice, resulting in four clus-ters by the time early bony fish (Oste-ichthyes) appeared some 415 millionyears ago.

We can recognize a hierarchy ofchange associated with Hox genesbetween and within phyla25. Arthropods

are distinguished from annelids by thepresence of two different Hox genes26,Ultrabithorax (Ubx) and abdominal A(abd-A), which diverged independentlyfrom a single gene in the common ances-tor of these phyla. Within the arthro-pods, what differentiates insects, myri-apods and crustaceans is not the numberofHoxgenes but the control of their areaof expression within the body. The ante-rior boundary of Ubx/abd-A (the genesare co-expressed) is correlated with tran-sitions in appendage morphology along

the anterioposterior axis (Fig. 3). TheHoxgenes control segmental identity byregulating the expression of downstreamtarget genes. In insects, absence of legson the abdomen results from repressionof the Distal-less (Dll) gene by the gene

PERSPECTIVES

Fig. 1. (a) Darwin2 used this figure to represent the patterns and rates of evolution at both the level of populations and species, and among higher taxa. The inter-

vals between the horizontal lines were given by Darwin as either thousands or tens of thousands of generations at the level of species or as millions to hundredsof millions of generations at the level of families and orders. The position along the horizontal axis indicates the degree of morphological difference. The angles

of the lines represent the rate of evolution; vertical lines indicate stasis. (b) A diagram of the fossil record of the major metazoan phyla showing their first appear-

ance in the late Proterozoic (Vendian) and early Paleozoic, and the persistence of basic body plans throughout the Phanerozoic. The essentially vertical orientation

of the clades indicates that each retained a basically similar body plan throughout its known history. The width of the lines is proportional to the number of fam-

ilies known from each geological period, and to some extent their anatomical diversity8. Other phyla that are known from the Cambrian, but have a comparatively

incomplete fossil record, include the Onychophora, Ctenophora, Priapulida, Phoronida and the Tardigrada.

a1

a2

a3

a4

a5

a6

a7

a8

a9

a10

a14

(a) (b)

q14 p14 b14 f14 o14 e14

m1

m2s2

m3

m4d4

i3

i4

m5d5 k5

m6k6

m7l7k7

m8l8k8

m9

m10

f6

f7

f8

f9

f10 e10

EDCBA

Neogene23

65

146

208

251

300

363

409

439

490

544

610

Porifera

Cnida

ria

Platyhelm

inthe

s

Anne

lida

Mollu

sca

Arthr

opoda

Brac

hiopo

da

Bryozo

a

Echin

odermata

Chorda

tes

Ce

nozoic

Mesozoic

Paleozoic

Paleogene

Cretaceous

Millionyearsago(Mya)

Jurassic

Triassic

Permian

Carboniferous

Devonian

Silurian

Ordovician

Cambrian

Vendian

m14

Trends in Ecology & Evolution


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TREE vol. 15, no. 1 January 2000 29

products of Ubxand abd-A, but this doesnot occur in centipedes or crustaceansbecause Hox-mediated repression has

not yet evolved in these classes.Changes in the number of Hoxgenes

and their control over the expression ofother genes can explain how distinctbody plans and appendages evolved inthe late Neoproterozoic and early Paleo-zoic, but they also provide a basis forexplaining other structural changesobserved throughout the subsequenthistory of life. Among vertebrates,changes in the area of expression of spe-cificHoxgenes have been used to explainthe transition between the fins of sar-copterygian fish and the limbs of Devon-

ian amphibians27, and differences in theshape and relative number of cervical,thoracic and lumbar vertebrae inamphibians, birds and mammals28. Otherstudies have demonstrated that morpho-logical differences between closelyrelated species and even polymorphismswithin populations can result from modi-fication in regulatory genes that influ-ence quantitative aspects of the expres-sion of a variety of structural genes.29

More broadly, the study ofHoxgeneshas revealed a far different pattern of

genetic control over structural features,throughout metazoan evolution, thanthose hypothesized by either mendelianor population genetics. Long-term evolu-tion is not simply the result of selectionof alternative alleles controlling specific

traits, or the progressive accumulationof new mutations in an additive fashion,as proposed by quantitative genetics. It

is now recognized that developmentinvolves a hierarchy of genetic control,including the precise timing and the posi-tion of expression of theHoxgenes them-selves, and the regulation of a cascade ofdownstream genes, together with inter-actions with the products of other Hoxgenes, commonly producing broadlypleiotrophic results in many tissuesand structures30,31. Evolutionary changesover a wide range of magnitudes canoccur by mutations at any point in thisgenetic complex.

Changes in the physical environmentThe evolution ofHoxgenes was a precon-dition for the origin of multicellularity inthe late Proterozoic, but additional fac-tors are necessary to explain the abruptradiation of advanced metazoan phyla inthe Early Cambrian. Major environmentalchanges were occurring during thisperiod, including substantial increases inthe availability of atmospheric oxygen32,which would have enabled the achieve-ment of larger body sizes and the for-mation of calcareous or phosphatic

skeletons in many lineages. The positionand configuration of the continents werealso undergoing major changes: in thelate Neoproterozoic, many of the conti-nents were grouped near the South Pole.Between 750 and 570 million years ago

PERSPECTIVES

Fig. 3. Expression domains of two Hox

genes, Ultrabithorax (Ubx) and abdominalA (abd-A), overlap (indicated by dark shading)

in an onychophoran and several arthropods.

The anterior boundary of Ubx/abd-A corre-

lates with transitions in appendage morphol-

ogy along the anterioposterior axis. In the

Onychophora, the boundary lies between the

second to last and last lobopod, in the cen-

tipede between the poison claw and the firstwalking leg, in Artemiabetween the gnathal

and thoracic segments that bear distinct

limbs, and in Drosophilabetween the last tho-

racic segment bearing legs and the abdomen.

Insects are unique in lacking legs on theabdomen. This results from the repression of

the gene Distal-less(Dll), by the genes Ubx

and abd-A, which would otherwise regulatethe formation of legs (from Ref. 26).

Drosophila

Artemia

Centipede

Onychophora

TrendsinEcology&Evolution

Fig. 2. Hoxclusters among multicellular animals, showing the degree of homology between selected phyla. Horizontal lines connect Hoxclusters, resulting from

tandem duplication of a single ancestralHoxgene. The hypothetical common protostome/deuterostome ancestor is thought to have given rise to all higher metazoans.

HoxaHoxd indicate the four Hoxclusters in vertebrates, resulting from two successive duplications of the ancestral chordate Hoxcluster (data from Refs 17,22,26).

Lox7Annelid ancestor pb Hox3 Lox6 Lox1/20 Lox5 Lox2 Lox4 Lox21

labOnychophora/arthropodancestor

pb Hox3 Dfd Scr ftz Antp Ubx AbdA AbdB

Protostome ancestor

Common protostome/deuterostome ancestor

1Ancestral chordate 2 3 4 5 6 7 8 9 10

a-1A Hoxa

Mouse Hoxclusters

a-2 a-3 a-4 a-5 a-6 a-7 a-9 a-10 a-11 a-13

b-1B Hoxb b-2 b-3 b-4 b-5 b-6 b-7 b-8 b-9 b-13

ParalogousgenesC Hoxc c-4 c-5 c-6 c-8 c-9 c-10 c-11 c-12 c-13

d-1D Hoxd d-3 d-4 d-8 d-9 d-10 d-11 d-12 d-13

1Hox groupsin vertebrates

2 3 4 5 6 7 8 9 10 11 12 13



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30 TREE vol. 15, no. 1 January 2000

there were several episodes of continen-

tal glaciation affecting many areas of theworld (Fig. 4a)5,33,34. However, at the endof the Proterozoic, the southern conti-nents began to move away from oneanother and the world climate began toameliorate. Not only higher tempera-tures but also the increase in the coast-lines and the areas of the continentalshelf, would have augmented the spaceavailable for marine life. These physicalfactors might have culminated, over a rel-atively short time, in conditions that fos-tered the differentiation of a multitude of

distinct adaptive strategies and bodypatterns that we see in the distinct meta-zoan phyla. What distinguished this timefurther was the absence of any pre-exist-ing complex multicellular animals thatcould act as predators or competitors of

the early members of the modern phyla.

The entire aquatic world was open forthem to conquer. The latter was a uniquephenomenon, but major changes in theposition of the continents have been acontinuing factor in the reshaping of thephysical environment and climate. Asstated by Knoll35: On the geological timescales on which evolution is played out,the physical development of our planetmay be a major engine of evolutionarychange.

Changes in the position and configu-ration of the continents have influenced

the patterns of evolution at many differ-ent time scales. The coalescence of thecontinents in the Permian is thought tohave been a major factor in the massextinction at the end of the Paleozoic36.Changes in global circulation led to pro-

gressive cooling in the Cenozoic, result-ing in long-term changes in the diet anddentition of Northern Hemisphere mam-mals, culminating in the origin of the arc-tic and tundra fauna of the Pleistocene37.Rifting of continental plates in thePliocene and Quaternary produced the

East African Great Lakes, within whichoccurred the explosive radiation of cich-lid fish over periods ranging from 5 mil-lion to as short as 12 000 years38. TheMilenkovitch cycles (i.e. changes in theearths axis of rotation and the eccentric-ity of its orbit) are associated with signif-icant climatic changes over intervals ofbetween 20 000 and 100 000 years, and ElNio produces measurable evolutionarychanges at time scales of less than adecade (e.g. changes in the length andheight of the bill of avian predators,associated with feeding on differenttypes of prey, which have differingabundance depending on the amount ofrainfall).

IntegrationFrom the time of Darwin, through the for-mulation of the evolutionary synthesis,evolution was studied and taught primarilyon the basis of what can be learned frommodern populations and species. Thefossil record documented the history oflife, but provided few unique concepts toexplain long-term, large-scale evolutionary

processes. Subsequently, knowledge of thesuccession of fossils covering 3.5 billionyears, plate tectonics and mass extinc-tions39 (Evolution on Planet Earth: TheImpact of the Physical Environment, TheLinnean Society of London, 67 May 1999)showed that physical changes during thehistory of the world have had a pro-found impact on its biota. More recently,knowledge from molecular biology hasrevealed how genes control developmentand how modifications in these genescan result in evolutionary changes of allmagnitudes. The present generation of

evolutionary biologists, whether trainedas paleontologists, molecular biologists orpopulation biologists, now has the oppor-tunity to integrate this information into anew synthesis, to guide evolutionary re-search and teaching in the next century(Box 1).

The flood of new techniques, infor-mation and concepts from molecular de-velopmental biology is already resultingin extensive cooperation with paleontol-ogists, reflected in joint studies of majormorphological changes and the origin of

new structures. This has proven especiallyeffective in understanding the radiationof metazoans in the Cambrian and theorigin and modification of appendages inboth arthropods and vertebrates27,40. Anew journal,Evolution and Development,

PERSPECTIVES

Fig. 4. The changing distribution of continents between the late Precambrian (late Neoproterozoic) and

the Cenozoic. (a) During the late Neoproterozoic, the continents were grouped close to the South Poleand the earth underwent a series of continental glaciations (shaded areas), with the ice sometimes

approaching sea level, even at tropical latitudes, suggesting severe cooling of the entire world. (b) In

the Permian, most of the continents were joined into a single land mass, resulting in great similarity of

land animals throughout the world. The coalescence of the continents might have restricted the heat

flow from the earths core, leading to explosive volcanism at the end of the Permian, which contributed

to the most drastic period of mass extinction in the history of life. (c) By the Late Cretaceous, the conti-

nents had drifted apart resulting in far greater endemism of terrestrial faunas, few barriers to oceanic

circulation and an equable climate over the entire earth. (d) By the middle Oligocene, Antarctica had

separated from both South America and Australia. This resulted in the formation of the Antarctic cir-cumpolar seaway, which isolated Antarctica thermally and led to the formation of the Antarctic icecap.

In the late Cenozoic, the Arctic ocean became effectively isolated from the Atlantic and Pacific oceans,

which might have contributed to the formation of the continental ice sheets that spread over North

America and Eurasia in the Pleistocene. [Maps (a), (c) and (d) from Ref. 5; map (b) from Ref. 45.]

Late Neoproterozoic(late Precambrian)

Siberia

SiberiaBaltica

BalticaSouth

America

SouthAmerica

SouthAmerica

SouthAmerica

SouthPole

(a) Late Permian(b)

Late Cretaceous(c) Middle Oligocene(d)

NorthAmerica

NorthAmerica

NorthAmerica

NorthAmerica

Africa

Africa

Africa

Africa

Austr

alia

Australia

Antarctica

Antarctica

Antarctica Antarctica

EuroasiaEuroasia

India

India

India

Arm

60S

30SEquator



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TREE vol. 15, no. 1 January 2000 31

has just been inaugurated and a new divi-sion, with this name, has been added tothe Society for Integrative and Compara-tive Biology. Numerous recent bookshave dealt with this subject7,20,30,41. Theneeds and the benefits of this associationwere summarized by Schlichting and

Pigliucci42: The time is ripe for evolution-ary theory to actively integrate develop-ment into its conceptual and experimen-tal arsenal, lest we squander a secondopportunity at a true synthesis.

However, as yet, there is relativelylittle integration of new evidence, fromeither molecular genetics or paleontol-ogy, into the publications on populationgenetics. This is especially conspicuousin the area of quantitative genetics, whichcontinues to treat polygenic traits in astatistical manner, as if they resultedfrom the additive effects of a large num-ber of essentially equivalent genes43.

Population genetics has also been slowto deal with the enigma that evolutionarychanges that are rapid in terms of geolog-ical time (such as the origin of tetrapodsand the evolution of horses) appear soslow, in comparison with the rates meas-ured in living populations, that they areindistinguishable from a random walk.Rapid rates of morphological change canbe observed from generation to generationas a result of rapidly changing selectioncoefficients44, but unidirectional selec-

tion is rarely maintained for a sufficienttime to result in continuing morphologicalor physiological modification. Over theduration of most species, the intensity anddirection of selection change repeatedly,either in an oscillating manner or in whatappears to be a random walk. Over short in-tervals, the rates of change accord well withexamples of the selection of alternativealleles emphasized in most textbooks. But,for much of the duration of the majority ofspecies there is relatively little net change,even over hundreds of thousands of years.The relatively rare events involving the

origin of major new taxa or significantmorphological divergence at the specieslevel require much greater than normalconsistency of directional selection.

Cooperation between populationgeneticists and paleontologists is neces-sary to provide a realistic bridge betweenthe rates and forces of evolution amongorganisms at the level of modern popu-lations and the patterns observed withingenera, families and orders. Researcherscould make use of field observations toestablish models that incorporate para-

meters such as: the duration of essen-tially unidirectional selection, which isnecessary for establishing recognizablechanges in the morphology and the phys-iology of a variety of traits in species withdifferent generation periods, population

sizes, habitats and ways of life; and therange of intensity of selection for varioustraits that can act more or less continu-ously on species for hundreds or thou-sands of generations without leading toextinction. These factors could be esti-mated over a wide range of time scales ina variety of organisms for which there isan extensive and well dated fossil record,such as many lineages of late Cenozoicmetazoans. Other models would be neces-sary for unicellular and clonal organisms.

However, over increasingly longer peri-odsof time, any model would break downbecause the nature of the organisms andtheir genetic systems changed beyondthe original parameters. Over the entirehistory of life, the nature of the earth andits atmosphere have changed to such anextent that none of the original types oforganisms could survive today. No gen-eral model could account for the massextinctions at the end of the Paleozoicand Mesozoic, or the subsequent changesin the earths biota.

A new evolutionary synthesis requires:

the integration of knowledge from allforms of life that have ever existed onearth; a thorough understanding of thegeological history of our planet; detailedknowledge of the changes in the biologyof development throughout all multicel-lular organisms; and an appreciation ofthe processes of genetic change, naturalselection and speciation as they can beobserved in modern populations.

AcknowledgementsI thank David Green for discussion andcomments on the manuscript, and

Elena Roman for preparing the illustrations.The referees provided many usefulsuggestions for improvement of themanuscript. Support for research wasprovided by the Natural Sciences andEngineering Research Council of Canada.

References1 Moore, W.S. (1999) Teaching neo-darwinism;

weak selection among evolution texts. Evolution

53, 635638

2 Darwin, C. (1859) On the Origin of Species by

Means of Natural Selection, Murray

3 Mayr, E. and Provine, W. (1980) The

Evolutionary Synthesis: Perspectives on the

Unification of Biology, Harvard University Press

4 Carroll, R.L. (1997) Patterns and Processes of

Vertebrate Evolution, Cambridge University

Press

5 van Ander, T.H. (1994) New Views on an Old

Planet(2nd edn), Cambridge University Press6 Ax, P. (1987) The Phylogenetic System, John

Wiley & Sons

7 Arthur, W. (1997) The Origin of Animal Body

Plans, Cambridge University Press

8 Benton, M.J., ed. (1993) The Fossil Record 2,

Chapman & Hall

9 Greenwood, P.H. (1974) The cichlid fishes of

Lake Victoria, East Africa. Bull. Br. Mus. (Nat.

Hist.) Zool. Suppl. 6, 1134

10 Valentine, J.W. et al. (1999) Fossils, molecules

and embryos: new perspectives on the

Cambrian explosion. Development126,

851859

11 Conway Morris, S. (1998) The Crucible of

Creation: The Burgess Shale and the Rise ofAnimals, Oxford University Press

12 Schopf, J.W. (1995) Disparate rates, different

fates: tempo and mode of evolution changed

from the Precambrian to the Phanerozoic. In

Tempo and Mode in Evolution(Fitch, W.M. and

Ayala, F.J., eds), pp. 4161, National Academy

of Sciences

13 Knoll, A.H. (1995) Proterozoic and Early

Cambrian protists: evidence of accelerating

evolutionary tempo. In Tempo and Mode in

Evolution(Fitch, W.M. and Ayala, F.J., eds), pp.

6383, National Academy of Sciences

14 Katz, L.A. (1998) Changing perspectives on the

origin of eukaryotes. Trends Ecol. Evol. 13,

493497

15 Lake, J.A. et al. (1999) Mix and match in the tree

of life. Science283, 20272028

16 Will, M.A. (1998) Crustacean disparity through

the Phanerozoic: comparing morphological and

stratigraphic data. Biol. J. Linn. Soc. 65, 455500

PERSPECTIVES

Box 1. Requirements for an expanded evolutionary synthesis

Recognition of the importance of physical events in the history of the earth as a driving force ofevolution, over time scales ranging from a decade or less (e.g. El Nio), through tens and hundredsof thousands of years (Milankovitch cycles and episodes of continental glaciation), to unique eventsthat re-set the pattern of evolution for the rest of the history of life (a progressive increase inatmospheric oxygen leading up to the Cambrian explosion and tectonic events associated with theend-Permian extinction).

Utilization of information, generated by molecular developmental biology, to investigate thewide range of evolutionary phenomena from the genetic control of body form in different phyla,through establishing the position and configuration of appendages in different clades within specificphyla, to the regulation of anatomical and physiological differences that are subject to selectionwithin species.

Employment of emerging knowledge of the mutual interaction of genes controlling quantitativetraits to formulate a truly descriptive, rather than a statistical, methodology for understandinghow natural selection controls their evolution.

Establishment of quantitative models to investigate the changing patterns of selection and structuralmodification in well known fossil lineages that record significant morphological change associatedwith adaptation to different environments and/or ways of life over varying time scales (e.g. theexplosive differentiation of placental mammals in the early Cenozoic and the continuing changesin the dentition of rodents associated with progressive cooling and drying in the late Cenozoic).

Recognition of the importance of horizontal genetic exchange throughout the history of life.


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Historically, it was recognized that lab-oratory selection experiments wouldbe valuable for testing evolutionaryhypotheses1,2 considerable progress hasbeen made in their design. For example,the importance of adequate line repli-

cation (multiple independent sub-popu-lations treated in the same manner) andof sufficient population size to avoidinbreeding when selecting on fitness-related characters has been established3.Although there are other useful genetic

approaches, selection experiments haveadvantageous features; these featuresinclude replication of selection treat-ments and controls, and a relatively highdegree of control of the conditions underwhich the experiment is conducted4.

Selection provides a genetic approach tomagnify phenotypic differences betweenselected lines and control lines, and itcan be used to measure direct and indi-rect (correlated) responses to selection5.Moreover, because selection experiments

allow for a relatively high degree of con-trol over the evolutionary process, theyprovide an opportunity to observe evo-

lution as it occurs and they can con-tribute to an understanding of physio-logical mechanisms involved in theresponse to selection4.

From an evolutionary perspective,the ability to study correlated responsesto selection is particularly valuable, be-cause these responses can indicate thepleiotropic basis of evolutionary con-straints resulting from trade-offs betweencharacters6. Watson and Hoffmann7

selected for increased resistance to coldstress in adultD. melanogasterand adultD. simulans, and found that an increase inadult cold resistance was accompaniedby a decrease in early fecundity in allreplicate lines of both species, thus sug-gesting the presence of a trade-off. Indi-rect responses to selection experimentscan be used to understand the mechanis-tic basis of tradeoffs by combining infor-mation on correlated changes in traitswith correlated changes in potentialmechanisms underlying the selection re-sponse. Importantly, correlated responsesto laboratory selection can reveal traitsand mechanisms whose association with

the response to selection was not antici-pated at the start of the experiment.In spite of the perceived value of labo-

ratory selection experiments, their use insome contexts is limited; this article willaddress two areas of general concern.

Laboratory selection experiments using

Drosophila: what do they really tell us?

Lawrence G. Harshman and Ary A. Hoffmann

Laboratory selection experiments using Drosophila, and other organisms, are widely used

in experimental biology. In particular, such experiments on D. melanogasterlife history

and stress-related traits have been instrumental in developing the emerging field of

experimental evolution. However, similar selection experiments often produce

inconsistent correlated responses to selection. Unfortunately, selection experiments are

vulnerable to artifacts that are difficult to control. In spite of these problems, selection

experiments are a valuable research tool and can contribute to our understanding of

evolution in natural populations.

Lawrence Harshman is at the School of Biological Sciences, University of Nebraska-Lincoln, Lincoln,

NE 68588, USA ([email protected]); Ary Hoffmann is at the Dept of Genetics and Evolution,

La Trobe University, Bundoora, Victoria 3083, Australia ([email protected]).

32 0169-5347/00/$ see front matter 2000 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(99)01756-5 TREE vol. 15, no. 1 January 2000

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PERSPECTIVES

towards a new evolutionary synthesis

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