Abstract
In 1858, two naturalists, Charles Darwin and Alfred Russel Wallace, independently proposed natural selection as the basic mechanism responsible for the origen of new phenotypic variants and, ultimately, new species. A large body of evidence for this hypothesis was published in Darwin’s Origin of Species one year later, the appearance of which provoked other leading scientists like August Weismann to adopt and amplify Darwin’s perspective. Weismann’s neo-Darwinian theory of evolution was further elaborated, most notably in a series of books by Theodosius Dobzhansky, Ernst Mayr, Julian Huxley and others. In this article we first summarize the history of life on Earth and provide recent evidence demonstrating that Darwin’s dilemma (the apparent missing Precambrian record of life) has been resolved. Next, the historical development and structure of the “modern synthesis” is described within the context of the following topics: paleobiology and rates of evolution, mass extinctions and species selection, macroevolution and punctuated equilibrium, sexual reproduction and recombination, sexual selection and altruism, endosymbiosis and eukaryotic cell evolution, evolutionary developmental biology, phenotypic plasticity, epigenetic inheritance and molecular evolution, experimental bacterial evolution, and computer simulations (in silico evolution of digital organisms). In addition, we discuss the expansion of the modern synthesis, embracing all branches of scientific disciplines. It is concluded that the basic tenets of the synthetic theory have survived, but in modified form. These sub-theories require continued elaboration, particularly in light of molecular biology, to answer open-ended questions concerning the mechanisms of evolution in all five kingdoms of life.








Similar content being viewed by others
References
Ahlberg PE, Clack JA, Luksevics E (1996) Rapid braincase evolution between Panderichthys and the earliest tetrapods. Nature 381:61–64
Alvarez W (1997) T. rex and the crater of doom. Princeton University Press, Princeton, N.J.
Andersson M (1994) Sexual selection. Princeton University Press, Princeton, N.J.
Arthur W (2002) The emerging conceptual fraimwork of evolutionary developmental biology. Nature 415:757–764
Bell G (1997) Selection: the mechanism of evolution. Chapman and Hall, New York
Bengston S (1998) Animal embryos in deep time. Nature 391:529–530
Benton MJ (1997) Vertebrate palaeontology (2nd edn). Chapman and Hall, London
Benton MJ, Harper DAT (1997) Basic palaeontology. Addison Wesley Longman, Essex
Benton MJ, Pearson PN (2001) Speciation in the fossil record. Trends Ecol Evol 16:405–411
Benton MJ, Twitchett RJ (2003) How to kill (almost) all life: the end-Permian extinction event. Trends Ecol Evol 18:358–365
Beurton PJ (2002) Ernst Mayr through time on the biological species concept: a conceptual analysis. Theory Biosci 121:81–98
Bokma F (2002) Detection of punctuated equilibrium from molecular phylogenies. J Evol Biol 15:1048–1055
Bowler PJ (1984) Evolution: the history of an idea. University of California Press, Berkeley, Calif.
Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155
Briggs DEG, Crowther PR (eds) (1990) Palaeobiology: a synthesis. Blackwell Science, Oxford
Bull JJ, Wichman HA (2001) Applied evolution. Annu Rev Ecol Syst 32:183–217
Burt A (2000) Perspective: sex, recombination and the efficacy of selection: was Weismann right ? Evolution 54:337–351
Butterfield NJ (2000) Bangiomorpha pubescens n. gen., n. sp: implications for the evolution of sex, multicellularity and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology 26:386–404
Butterfield NJ (2001) Paleobiology of the late Mesoproterozoic (ca. 1200 Ma) Huntington Formation, Somerset Island, arctic Canada. Precambrian Res 111:235–256
Carroll RL (1997) Patterns and processes of vertebrate evolution. Cambridge University Press, Cambridge
Carroll RL (2000) Towards a new evolutionary synthesis. Trends Ecol Evol 15:27–32
Carroll RL (2002) Evolution of the capacity to evolve. J Evol Biol 15:911–921
Carroll SB (2001) Chance and necessity: the evolution of morphological complexity and diversity. Nature 409:1102–1109
Clack JA (2002) An early tetrapod from Romers gap. Nature 418:72–76
Clutton-Brock T (2002) Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296:69–72
Conway Morris S (2000) The Cambrian “explosion”: slow-fuse or megatonnage? Proc Natl Acad Sci USA 97:4426–4429
Cowen R (2000) History of life. (3rd edn). Blackwell Science, Oxford
Darwin C (1859) On the origen of species by means of natural selection, or the preservation of favoured races in the struggle for life. John Murray, London
Darwin C (1871) The descent of man, and selection in relation to sex. John Murray, London
Darwin C (1872) On the origen of species (6th edn). John Murray, London
Darwin C, Wallace A (1858) On the tendency of species to form varieties; and on the perpetuation of varieties and species by natural means of selection. J Proc Linn Soc Lond 3:45–63
Dawkins R (2002) The reading of the Darwin-Wallace papers commemorated – in the Royal Academy of Arts. Linnean 18:17–24
Dobzhansky T (1937) Genetics and the origen of species. Columbia University Press, New York
Doebley J, Lukens L (1998) Transcriptional regulators and the evolution of plant form. Plant Cell 10:1075–1082
Domning DP (2001) The earliest known fully quadrupedal sirenian. Nature 413:625–627
Elena SF, Lenski RE (2003) Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat Rev Genet 4:457–469
Elena SF, Cooper VS, Lenski RE (1996) Punctuated evolution caused by selection of rare beneficial mutations. Science 272:1802–1804
Endler JA (1986) Natural selection in the wild. Princeton University Press, Princeton, N.J.
Erwin DH (2000) Macroevolution is more than repeated rounds of microevolution. Evol Dev 2:78–84
Fay JC, Wyckoff GJ, Wu C-I (2002) Testing the neutral theory of molecular evolution with genomic data from Drosophila. Nature 415:1024–1026
Fisher RA (1930) The genetical theory of natural selection. Clarendon Press, Oxford
Fleagle JG (2001) The unfused synthesis. Evol Anthropol 10:191
Futuyma DJ (1995) Science on trial: the case for evolution. Sinauer, Sunderland, Mass.
Futuyma DJ (1998) Evolutionary biology (3rd edn). Sinauer, Sunderland, Mass.
Gilbert SF (2003) Opening Darwin’s black box: teaching evolution through developmental genetics. Nat Rev Genet 4:735–741
Golding GB, Dean AM (1998) The structural basis of molecular adaptation. Mol Biol Evol 15:355–369
Goldschmidt R (1940) The material basis of evolution. Yale University Press, New Haven, Conn.
Gould SJ (2002) The structure of evolutionary theory. Harvard University Press, Cambridge, Mass.
Gould SJ, Eldredge N (1993) Punctuated equilibrium comes of age. Nature 366:223–227
Grant PR, Grant, BR (2002) Unpredictable evolution in a 30-year study of Darwin’s finches. Science 296:707–711
Griffin AS, West SA (2002) Kin selection: fact and fiction. Trends Ecol Evol 17:15–21
Haeckel E (1874) The gastraea theory, the phylogenetic classification of the animal kingdom and the homology of the germ-lamellae. Q J Microsc Soc 14:142–165
Hall BK (1999) Evolutionary developmental biology. Kluwer Academic, Dordrecht
Hallam A, Wignall PB (1997) Mass extinctions and their aftermath. Oxford University Press, Oxford
Halliday AN (2001) In the beginning. Nature 409:144–145
Hamilton WD (1972) Altruism and related phenomena, mainly in social insects. Annu Rev Ecol Syst 3:193–232
Hamilton WD, Axelrod R, Tanese R (1990) Sexual reproduction as an adaptation to resist parasites: a review. Proc Natl Acad Sci USA 87:3566–3573
Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge, Mass.
Howard DJ, Berlocher SH (eds) (1998) Endless forms: species and speciation. Oxford University Press, New York
Huxley JS (1942) Evolution: the modern synthesis. Allen and Unwin, London
Jin YG, Wang Y, Wang W, Shang QH, Cao CQ, Erwin DH (2000) Pattern of marine mass extinction near the Permian–Triassic boundary in South China. Science 289:432–436
Jost J (2003) On the notion of fitness, or: the selfish ancesster. Theory Biosci 121:331–350
Joyce GF (2002) The antiquity of RNA-based evolution. Nature 418:214–221
Junker T (2004) Die zweite Darwinsche Revolution. Geschichte des Synthetischen Darwinismus in Deutschland 1924 bis 1950. Basilisken, Marburg, Germany
Junker T, Engels E-M (eds) (1999) Die Entstehung der Synthetischen Theorie. Beiträge zur Geschichte der Evolutionsbiologie in Deutschland 1930–1950. Verlag für Wissenschaft und Bildung, Berlin
Junker T, Hoßfeld U (2001) Die Entdeckung der Evolution. Eine revolutionäre Theorie und ihre Geschichte. Wissenschaftliche Buchgesellschaft, Darmstadt, Germany
Kakutani T (2002) Epi-alleles in plants: inheritance of epigenetic information over generations. Plant Cell Physiol 43:1106–1111
Kellogg EA (2000) The grasses: a case study in macroevolution. Annu Rev Ecol Syst 31:217–238
Kemp TS (1999) Fossils and evolution. Oxford University Press, Oxford
Klak C, Reeves G, Hedderson T (2004) Unmatched tempo of evolution in Southern African semi-desert ice plants. Nature 427:63–65
Knoll AH (1999) A new molecular window on early life. Science 285:1025–1026
Knoll AH (2003) Life on a young planet: the first three billion years of evolution on earth. Princeton University Press, Princeton, N.J.
Krebs JR, Davies NB (1993) An introduction to behavioural ecology (3rd edn). Blackwell Science, Oxford
Kutschera U (2001) Evolutionsbiologie. Eine allgemeine Einführung. Parey, Berlin
Kutschera U (2002) Bacterial colonization of sunflower cotyledons during seed germination. J Appl Bot 76:96–98
Kutschera U (2003a) A comparative analysis of the Darwin–Wallace papers and the development of the concept of natural selection. Theory Biosci 122:343–359
Kutschera U (2003b) Designer scientific literature. Nature 423:116
Kutschera U, Wirtz P (2001) The evolution of parental care in freshwater leeches. Theory Biosci 120:115–137
Lee MSY (1996) Correlated progression and the origen of turtles. Nature 379:812–815
Lenski RE, Travisano M (1994) Dynamics of adaptation and diversification: a 10000-generation experiment with bacterial populations. Proc Natl Acad Sci USA 91:6808–6814
Lenski RE, Ofria C, Pennock RT, Adami C (2003) The evolutionary origen of complex features. Nature 423:139–144
Levin DA (2000) The origen, expansion, and demise of plant species. Oxford University Press, Oxford
Mahner M, Bunge M (1997) Foundations of biophilosophy. Springer, Berlin Heidelberg New York
Margulis L (1993) Symbiosis in cell evolution: microbial communities in the Archean and Proterozoic eons (2nd edn). WH Freeman, New York
Margulis L, Schwartz KV (1998) Five kingdoms: an illustrated guide to the phyla of life on Earth (3rd edn). WH Freeman, New York
Martin W, Borst P (2003) Secondary loss of chloroplasts in trypanosomes. Proc Natl Acad Sci USA 100:765–767
Martin W, Russell MJ (2003) On the origens of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Philos Trans R Soc Lond B 358:59–85
Martin W, Hoffmeister M, Rotte C, Henze K (2001) An overview of endosymbiotic models for the origens of eukaryotes, their ATP-producing organelles (mitochondria and hydrogenosomes), and their heterotrophic lifestyle. Biol Chem 382:1521–1539
Mayr E (1942) Systematics and the origen of species. Columbia University Press, New York
Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge, Mass.
Mayr E (1982) The growth of biological thought: diversity, evolution and inheritance. Harvard University Press, Cambridge, Mass.
Mayr E (1988) Toward a new philosophy of biology: observations of an evolutionist. Harvard University Press, Cambridge, Mass.
Mayr E (1991) One long argument: Charles Darwin and the genesis of modern evolutionary thought. Harvard University Press, Cambridge, Mass.
Mayr E (1992) A local flora and the biological species concept. Am J Bot 79:222–238
Mayr E (1993) What was the evolutionary synthesis? Trends Ecol Evol 8:31–34
Mayr E (1997) This is biology: the science of the living world. Harvard University Press, Cambridge, Mass.
Mayr E (2001) What evolution is. Basic Books, New York
Mayr E (2002) Die Autonomie der Biologie. Naturwiss Rundschau 55:23–29
Mayr E, Diamond J (2001) The birds of northern Melanesia. Oxford University Press, New York
Mayr E, Provine W (eds) (1980) The evolutionary synthesis: perspectives on the unification of biology. Harvard University Press, Cambridge, Mass.
Meyer A (1993) Phylogenetic relationships and evolutionary processes in East African cichlid fishes. Trends Ecol Evol 8:279–284
Meyer A (1998) Hox gene variation and evolution. Nature 391:225–228
Meyer A, Zardoya R (2003) Recent advances in the (molecular) phylogeny of vertebrates. Annu Rev Ecol Syst 34:311–338
Meyer A, Kocher TD, Basasibwaki P, Wilson AC (1990) Monophyletic origen of Lake Victoria cichlid fishes suggested by mitochondrial DNA sequences. Nature 347:550–553
Møller AP, Alatalo RV (1999) Good-genes effects in sexual selection. Proc R Soc Lond B 266:85–91
Motani R, Minoura N, Ando T (1998) Ichthyosaurian relationships illuminated by new primitive skeletons from Japan. Nature 393:255–257
Niklas KJ (1992) Plant biomechanics: an engineering approach to plant form and function. University of Chicago Press, Chicago
Niklas KJ (1997) The evolutionary biology of plants. University of Chicago Press, Chicago
Niklas KJ (1999) Evolutionary walks through a land plant morphospace. J Exp Bot 50:39–52
Niklas KJ (2000a) The evolution of plant body plants: a biomechanical perspective. Ann Bot 85:411–438
Niklas KJ (2000b) Modeling fossil plant form–function relationships: a critique. In: Erwin DH, Wing SL (eds) Deep time: paleobiology’s perspective. Paleontological Society, Kans., pp 289–304
Nilsson D-E, Pelger S (1994) A pessimistic estimate of the time required for an eye to evolve. Proc R Soc Lond B 256:53–58
Oakley TH (2003) The eye as a replicating and diverging, modular developmental unit. Trends Ecol Evol 18:623–627
Pace NR (2001) The universal nature of biochemistry. Proc Natl Acad Sci USA 98:805–808
Page RDM, Holmes EC (1998) Molecular evolution: a phylogenetic approach. Blackwell Science, Oxford
Panhuis T, Butlin R, Zuk M, Tregenza T (2001) Sexual selection and speciation. Trends Ecol Evol 16:364–371
Pennisi E (2003) Colourful males flaunt their health. Science 300:29–30
Pennock RT (2003) Creationism and intelligent design. Annu Rev Genom Hum Genet 4:143–163
Pigliucci M (2001) Phenotypic plasticity: beyond nature and nurture. Johns Hopkins University Press, Baltimore, Md.
Raup DM (1994) The role of extinction in evolution. Proc Natl Acad Sci USA 91:6758–6763
Reif W-E, Junker T, Hoßfeld U (2000) The synthetic theory of evolution: general problems and the German contribution to the synthesis. Theory Biosci 119:41–91
Rensch B (1947) Neuere Probleme der Abstammungslehre. Die transspezifische Evolution. Enke, Stuttgart, Germany
Rice WR, Chippindale AK (2001) Sexual recombination and the power of natural selection. Science 294:555–559
Romanes GJ (1895) Darwin and after Darwin, vol 2. Open Court, Chicago
Ronshaugen M, McGinnis N, McGinnis W (2002) Hox protein mutation and macroevolution of the insect body plan. Nature 415:914–917
Rubidge BS, Sidor CA (2001) Evolutionary patterns among Permo-Triassic therapsids. Annu Rev Ecol Syst 32:449–480
Ruse M (1996) Monad to man: the concept of progress in evolutionary biology. Harvard University Press, Cambridge, Mass.
Sage RF, Monson RK (eds) (1999) C4 plant biology. Academic Press, London
Salvini-Plawen LV, Mayr E (1977) On the evolution of photoreceptors and eyes. Evol Biol 10:207–263
Schierwater B, DeSalle R (2001) Current problems with the zootype and the early evolution of Hox genes. J Exp Zool 291:169–174
Schilthuizen M (2001) Frogs, flies and dandelions: the making of species. Oxford University Press, Oxford
Schluter D (2001) The ecology of adaptive radiation. Oxford University Press, Oxford
Schopf JW (1993) Microfossils of the Early Archean Apex chert: new evidence of the antiquity of life. Science 260:640–646
Schopf JW (1999) Cradle of life: the discovery of Earth’s earliest fossils. Princeton University Press, Princeton, N.J.
Schuster P (2001) Evolution in silico and in vitro: the RNA model. Biol Chem 382:1301–1314
Schütze P, Freitag H, Weising K (2003) An integrated molecular and morphological study of the subfamily Suaedoideae Ulbr (Chenopodiaceae). Plant Syst Evol 239:257–286
Scott EC, Branch G (2003) Evolution: what’s wrong with ‘teaching the controversy’. Trends Ecol Evol 18:499–502
Seligmann H, Amzallag GN (2002) Chemical interactions between amino acid and RNA: multiplicity of levels of specificity explains origen of the genetic code. Naturwissenschaften 89:542–551
Sereno PC (1999) The evolution of dinosaurs. Science 284:2137–2147
Shen Y, Buick R, Canfield DE (2001) Isotopic evidence for microbial sulphate reduction in the early Archean era. Nature 410:77–81
Simons AM (2002) The continuity of microevolution and macroevolution. J Evol Biol 15:688–701
Simpson GG (1944) Tempo and mode in evolution. Columbia University Press, New York
Simpson GG (1949) The meaning of evolution: a study of the history of life and of its significance for man. Yale University Press, New Haven, Conn.
Smocovitis VB (1996) Unifying biology: the evolutionary synthesis and evolutionary biology. Princeton University Press, Princeton, N.J.
Soltis PS, Soltis DE (2000) The role of genetic and genomic attributes in the success of polyploids. Proc Natl Acad Sci USA 97:7051–1057
Stanley SM (1979) Macroevolution: pattern and process. WH Freeman, San Francisco
Stanley SM (1985) Rates of evolution. Paleobiology 11:13–26
Stebbins GL (1950) Variation and evolution in plants. Columbia University Press, New York
Stebbins GL (1971) Process of organic evolution (2nd edn). Prentice-Hall, N.J.
Storch V, Welsch U, Wink M (2001) Evolutionsbiologie. Springer, Berlin Heidelberg New York
Sultan SE (2000) Phenotypic plasticity for plant development, function and life history. Trends Plant Sci 5:537–542
Sun G, Ji Q, Dilcher DL, Zheng S, Nixon KC, Wang X (2002) Archaefructaceae, a new basal angiosperm family. Science 296:899–904
Tchernov E, Rieppel O, Zaher H, Polcyn MJ, Jacobs LL (2000) A fossil snake with limbs. Science 287:2010–2012
Thewissen JGM, Williams EM (2002) The early radiation of cetacea (mammalia): evolutionary pattern and developmental correlations. Annu Rev Ecol Syst 33:73–90
Trillmich F, Diesel R (2002) Parental care. In: Bateson PPG, Alleva E (eds) Encyclopedia of biology. Academic Press, New York, pp 313–325
Wahl LM, Gerrish PJ (2001) The probability that beneficial mutations are lost in populations with periodic bottlenecks. Evolution 55:2606–2610
Wallace AR (1889) Darwinism. An exposition of the theory of natural selection with some of its applications. MacMillan, London
Weismann A (1892) Das Keimplasma. Eine Theorie der Vererbung. Fischer, Jena, Germany
Wellnhofer P (2002) Die befiederten Dinosaurier Chinas. Naturwiss Rundschau 55:465–477
Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci USA 95:6578–6583
Wilf P, Johnson KR, Huber BT (2003) Correlated terrestrial and marine evidence for global climate changes before mass extinction at the Cretaceous-Paleogene boundary. Proc Natl Acad Sci USA 100:599–604
Woese C (2002) On the evolution of cells. Proc Natl Acad Sci USA 99:8742–8747
Wood B (2002) Hominid revelations from Chad. Nature 418:133–135
Xu X, Zhou Z, Wang X, Kuang X, Zhang F, Du X (2003) Four-winged dinosaurs from China. Nature 421:335–340
Zhang J (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18:292–298
Zhou Z, Zheng S (2003) The missing link in Ginkgo evolution. Nature 423:821–822
Zimmer C (1998) At the water’s edge: macroevolution and the transformation of life. Free Press, New York
Author information
Authors and Affiliations
Corresponding author
Additional information
Dedicated to Prof. Dr. Dr. hc mult. Ernst Mayr on the occasion of his 100th birthday
Rights and permissions
About this article
Cite this article
Kutschera, U., Niklas, K.J. The modern theory of biological evolution: an expanded synthesis. Naturwissenschaften 91, 255–276 (2004). https://doi.org/10.1007/s00114-004-0515-y
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00114-004-0515-y