Skip to main content
Log in

Saltational evolution: hopeful monsters are here to stay

  • Original Paper
  • Published:
Theory in Biosciences Aims and scope Submit manuscript

Abstract

Since 150 years it is hypothesized now that evolution always proceeds in a countless number of very small steps (Darwin in On the origin of species by means of natural selection or the preservation of favoured races in the struggle of life, Murray, London, 1859), a view termed “gradualism”. Few contemporary biologists will doubt that gradualism reflects the most frequent mode of evolution, but whether it is the only one remains controversial. It has been suggested that in some cases profound (“saltational”) changes may have occurred within one or a few generations of organisms. Organisms with a profound mutant phenotype that have the potential to establish a new evolutionary lineage have been termed “hopeful monsters”. Recently I have reviewed the concept of hopeful monsters in this journal mainly from a historical perspective, and provided some evidence for their past and present existence. Here I provide a brief update on data and discussions supporting the view that hopeful monsters and saltational evolution are valuable biological concepts. I suggest that far from being mutually exclusive scenarios, both gradual and saltational evolution are required to explain the complexity and diversity of life on earth. In my view, gradual changes represent the usual mode of evolution, but are unlikely to be able to explain all key innovations and changes in body plans. Saltational changes involving hopeful monsters are probably very exceptional events, but since they have the potential to establish profound novelties sometimes facilitating adaptive radiations, they are of quite some importance, even if they would occur in any evolutionary lineage less than once in a million years. From that point of view saltational changes are not more bizarre scenarios of evolutionary change than whole genome duplications, endosymbiosis or impacts of meteorites. In conclusion I argue that the complete dismissal of saltational evolution is a major historical error of evolutionary biology tracing back to Darwin that needs to be rectified.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Akam M (1998) Hox genes, homeosis and the evolution of segment identity: no need for hopeless monsters. Int J Dev Biol 42:445–451

    PubMed  CAS  Google Scholar 

  • Albert VA, Oppenheimer DG, Lindqvist C (2002) Pleiotropy, redundancy and the evolution of flowers. Trends Plant Sci 7:297–301

    Article  PubMed  CAS  Google Scholar 

  • Arthur W (2002) The emerging conceptual framework of evolutionary developmental biology. Nature 415:757–764

    PubMed  CAS  Google Scholar 

  • Barabé D, Lacroix C, Jeune B (2008) Quantitative developmental analysis of homeotic changes in the inflorescence of Philodendron (Araceae). Ann Bot 101:1027–1034

    Article  PubMed  Google Scholar 

  • Bateman RM, DiMichele WA (1994) Saltational evolution of form in vascular plants: a neoGoldschmidtian synthesis. In: Ingram DS, Hudson A (eds) Shape and form in plants and fungi. Academic Press, London, pp 63–102

    Google Scholar 

  • Bateman RM, DiMichele WA (2002) Generating and filtering major phenotypic novelties: neoGoldschmidtian saltation revisited. In: Cronk QCB, Bateman RM, Hawkins JA (eds) Developmental genetics and plant evolution. Taylor & Francis, London, pp 109–159

    Google Scholar 

  • Baum DA, Donoghue MJ (2002) Transference of function, heterotopy and the evolution of plant development. In: Cronk QCB, Bateman RM, Hawkins JA (eds) Developmental genetics and plant evolution. Taylor & Francis, London, pp 52–69

    Google Scholar 

  • Baum DA, Hileman LC (2006) A developmental genetic model for the origin of the flower. In: Ainsworth C (ed) Flowering and its manipulation. Blackwell Publishing, Sheffield, pp 3–27

    Google Scholar 

  • Carroll SB (2001) Chance and necessity: the evolution of morphological complexity and diversity. Nature 409:1102–1109

    Article  PubMed  CAS  Google Scholar 

  • Chagas-Junior A, Edgecombe GD, Minelli A (2008) Variability in trunk segmentation in the centipede order Scolopendromorpha: a remarkable new species of Scolopendropsis Brandt (Chilopoda: Scolopendridae) from Brazil. Zootaxa 1888:36–46

    Google Scholar 

  • Citerne HL, Pennington RT, Cronk QCB (2006) An apparent reversal in floral symmetry in the legume Cadia is a homeotic transformation. Proc Natl Acad Sci USA 103:12017–12020

    Article  PubMed  CAS  Google Scholar 

  • Crepet WL (2000) Progress in understanding angiosperm history, success, and relationships: Darwin’s abominable “perplexing phenomenon”. Proc Natl Acad Sci USA 97:12939–12941

    Article  PubMed  CAS  Google Scholar 

  • Crepet WL, Niklas KJ (2009) Darwin’s second “abominable mystery”: why are there so many angiosperm species? Am J Bot 96:366–381

    Article  Google Scholar 

  • Darwin C (1859) On the origin of species by means of natural selection or the preservation of favoured races in the struggle of life. Murray, London

    Google Scholar 

  • Dietrich MR (2000) From hopeful monsters to homeotic effects: Richard Goldschmidt’s integration of development, evolution and genetics. Am Zool 40:738–747

    Article  Google Scholar 

  • Dietrich MR (2003) Richard Goldschmidt: hopeful monsters and other ‘heresies’. Nat Rev Genet 4:68–74

    Article  PubMed  CAS  Google Scholar 

  • Dobzhansky T (1937) Genetics and the origin of species. Columbia University Press, New York

    Google Scholar 

  • Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance in maize. Nature 386:485–488

    Article  PubMed  CAS  Google Scholar 

  • Erwin DH (2000) Macroevolution is more than just repeated rounds of microevolution. Evol Dev 2:78–84

    Article  PubMed  CAS  Google Scholar 

  • Frohlich MW (2003) An evolutionary scenario for the origin of flowers. Nat Rev Genet 4:559–566

    Article  PubMed  CAS  Google Scholar 

  • Frohlich MW, Parker DS (2000) The mostly male theory of flower evolutionary origins: from genes to fossils. Syst Bot 25:155–170

    Article  Google Scholar 

  • Gailing O, Bachmann K (2000) The evolutionary reduction of microsporangia in Microseris (Asteraceae): transition genotypes and phenotypes. Plant Biol 2:455–461

    Article  Google Scholar 

  • Géant É, Mouchel-Vielh E, Coutanceau J-P, Ozouf-Costaz C, Deutsch JS (2006) Are Cirripedia hopeful monsters? Cytogenetic approach and evidence for a Hox gene cluster in the cirripede crustacean Sacculina carcini. Dev Genes Evol 216:443–449

    Article  PubMed  Google Scholar 

  • Gilbert SF, Opitz JM, Raff RA (1996) Resynthesizing evolutionary and developmental biology. Dev Biol 173:357–372

    Article  PubMed  CAS  Google Scholar 

  • Goldschmidt R (1933) Some aspects of evolution. Science 78:539–547

    Article  PubMed  Google Scholar 

  • Goldschmidt R (1940) The material basis of evolution. Yale University Press, New Haven

    Google Scholar 

  • Gould SJ (1977a) The return of hopeful monsters. Nat Hist 86(6):24–30

    Google Scholar 

  • Gould SJ (1977b) Ontogeny and phylogeny. Harvard University Press, Cambridge

    Google Scholar 

  • Gould SJ, Eldredge N (1993) Punctuated equilibrium comes of age. Nature 366:223–227

    Article  PubMed  CAS  Google Scholar 

  • Grimmer JC, Holland ND (1990) The structure of a sessile, stalkless crinoid (Holopus rangii). Acta Zool 71:61–67

    Article  Google Scholar 

  • Haag ES, True JR (2001) From mutants to mechanisms? Assessing the candidate gene paradigm in evolutionary biology. Evolution 55:1077–1084

    PubMed  CAS  Google Scholar 

  • Hintz M, Bartholmes C, Nutt P, Ziermann J, Hameister S, Neuffer B, Theißen G (2006) Catching a ‘hopeful monster’: shepherd’s purse (Capsella bursa-pastoris) as a model system to study the evolution of flower development. J Exp Bot 57:3531–3542

    Article  PubMed  CAS  Google Scholar 

  • Junker T (2004) Die zweite Darwinsche Revolution. Geschichte des Synthetischen Darwinismus in Deutschland 1924 bis 1950 (Acta Biohistorica, Bd. 8). Basilisken-Presse, Marburg

    Google Scholar 

  • Junker T, Hoßfeld U (2001) Die Entdeckung der Evolution. Eine revolutionäre Theorie und ihre Geschichte. Wissenschaftliche Buchgesellschaft, Darmstadt

    Google Scholar 

  • Kanno A, Saeki H, Kameya T, Saedler H, Theissen G (2003) Heterotopic expression of class B floral homeotic genes supports a modified ABC model for tulip (Tulipa gesneriana). Plant Mol Biol 52:831–841

    Article  PubMed  CAS  Google Scholar 

  • Kellogg EA (2000) The grasses: a case study in macroevolution. Annu Rev Ecol Syst 31:217–238

    Article  Google Scholar 

  • Kirschner MW, Gerhart JC (2005) The plausibility of life—resolving Darwin’s dilemma. Yale University Press, New Haven

    Google Scholar 

  • Kuratani S (2005) Developmental studies of the lamprey and hierarchical evolutionary steps towards the acquisition of the jaw. J Anat 207:489–499

    PubMed  Google Scholar 

  • Leitch AR, Leitch IJ (2007) Genomic plasticity and the diversity of polyploid plants. Science 320:481–483

    Article  CAS  Google Scholar 

  • Lenski RE, Ofria C, Pennock RT, Adami C (2003) The evolutionary origin of complex features. Nature 423:139–144

    Article  PubMed  CAS  Google Scholar 

  • Levit GS, Meister K, Hoßfeld U (2008) Alternative evolutionary theories: a historical survey. J Bioecon 10:71–96

    Article  Google Scholar 

  • Lewis EB (1994) Homeosis: the first 100 years. Trends Genet 10:341–343

    Article  PubMed  CAS  Google Scholar 

  • Li C, Wu X-C, Rieppel O, Wang L-T, Zhao L-J (2008) An ancestral turtle from the Late Triassic of southwestern China. Nature 456:497–501

    Article  PubMed  CAS  Google Scholar 

  • Mallet J (2007) Hybrid speciation. Nature 446:279–283

    Article  PubMed  CAS  Google Scholar 

  • Martin W, Hoffmeister M, Rotte C, Henze K (2001) An overview of endosymbiotic models for the origin of eukaryotes, their ATP-producing organelles (mitochondria and hydrogenosomes), and their heterotrophic lifestyle. Biol Chem 382:1521–1539

    Article  PubMed  CAS  Google Scholar 

  • Mayr E (1942) Systematics and the origin of species. Columbia University Press, New York

    Google Scholar 

  • Mayr E, Provine WB (1980) The evolutionary synthesis. Harvard University Press, Cambridge

    Google Scholar 

  • Meyerowitz EM, Smyth DR, Bowman JL (1989) Abnormal flowers and pattern formation in floral development. Development 106:209–217

    Google Scholar 

  • Mondragón-Palomino M, Theißen G (2008) MADS about the evolution of orchid flowers. Trends Plant Sci 13:51–59

    PubMed  Google Scholar 

  • Mondragón-Palomino M, Theissen G (2009, in press) Why are orchid flowers so diverse? Reduction of evolutionary constraints by paralogues of class B floral homeotic genes. Ann Bot. doi:10.1093/aob/mcn258

  • Moritz DML, Kadereit JW (2001) The genetics of evolutionary change in Senecio vulgaris L.: a QTL mapping approach. Plant Biol 3:544–552

    Article  CAS  Google Scholar 

  • Mosbrugger V (1989) Gibt es sprunghafte Evolution? Formen und Mechanismen der transspezifischen Evolution bei Pflanzen. Biol Unserer Zeit 19(1):1–8

    Article  Google Scholar 

  • Müller GB, Wagner GP (1991) Novelty in evolution: restructuring the concept. Annu Rev Ecol Syst 22:229–256

    Article  Google Scholar 

  • Nagashima H, Kuraku S, Uchida K, Ohya YK, Narita Y, Kuratani S (2007) On the carapacial ridge in turtle embryos: its developmental origin and the chelonian body plan. Development 134:2219–2226

    Article  PubMed  CAS  Google Scholar 

  • Nutt P, Ziermann J, Hintz M, Neuffer B, Theißen G (2006) Capsella as a model system to study the evolutionary relevance of floral homeotic mutants. Plant Syst Evol 259:217–235

    Article  Google Scholar 

  • Ohya YK, Kuraku S, Kuratani S (2005) Hox code in embryos of Chinese soft-shelled turtle Pelodiscus sinensis correlates with the evolutionary innovation in the turtle. J Exp Zool Mol Dev Evol 304B:107–118

    Article  CAS  Google Scholar 

  • Patterson C (1988) Homology in classical and molecular biology. Mol Biol Evol 5:603–625

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Reisz RR, Head JJ (2008) Turtle origins out to sea. Nature 456:450–451

    Article  PubMed  CAS  Google Scholar 

  • Riedl R (1977) A systems-analytical approach to macro-evolutionary phenomena. Q Rev Biol 52:351–370

    Article  PubMed  CAS  Google Scholar 

  • Rieppel O (2001) Turtles as hopeful monsters. Bioessays 23:987–991

    Article  PubMed  CAS  Google Scholar 

  • Ronse De Craene LP (2003) The evolutionary significance of homeosis in flowers: a morphological perspective. Int J Plant Sci 164:S225–S235

    Article  Google Scholar 

  • Ronse De Craene LP (2007) Are petals sterile stamens or bracts? The origin and evolution of petals in the core eudicots. Ann Bot 100:621–630

    Article  PubMed  Google Scholar 

  • Rudall PJ, Bateman RM (2002) Roles of synorganisation, zygomorphy and heterotopy in floral evolution: the gynostemium and labellum of orchids and other lilioid monocots. Biol Rev 77:403–441

    Article  PubMed  Google Scholar 

  • Rudall PJ, Bateman R (2003) Evolutionary change in flowers and inflorescences: evidence from naturally occurring terata. Trends Plant Sci 8:76–82

    Article  PubMed  CAS  Google Scholar 

  • Rutishauser R, Isler B (2001) Developmental genetics and morphological evolution of flowering plants, especially bladderworts (Utricularia): fuzzy Arberian morphology complements classical morphology. Ann Bot 88:1173–1202

    Article  Google Scholar 

  • Sattler R (1988) Homeosis in plants. Am J Bot 75:1606–1617

    Article  Google Scholar 

  • Simpson GG (1944) Tempo and mode in evolution. Columbia University Press, New York

    Google Scholar 

  • Stuessy TF (2004) A transitional-combinational theory for the origin of angiosperms. Taxon 53:3–16

    Article  Google Scholar 

  • Tautz D (1998) Debatable homologies. Nature 395:17–19

    Article  PubMed  CAS  Google Scholar 

  • Theißen G (2005) Birth, life and death of developmental control genes: new challenges for the homology concept. In: Richter S, Olsson L (eds) Evolutionary developmental biology: new challenges to the homology concept? Theory Biosci 124:199–212

  • Theißen G (2006) The proper place of hopeful monsters in evolutionary biology. Theory Biosci 124:349–369

    Article  PubMed  Google Scholar 

  • Theißen G, Becker A (2004) Gymnosperm orthologues of class B floral homeotic genes and their impact on understanding flower origin. Crit Rev Plant Sci 23:129–148

    Article  CAS  Google Scholar 

  • Theißen G, Melzer R (2007) Molecular mechanisms underlying origin and diversification of the angiosperm flower. Ann Bot 100:603–619

    Article  PubMed  Google Scholar 

  • Theißen G, Becker A, Di Rosa A, Kanno A, Kim JT, Münster T, Winter K-U, Saedler H (2000) A short history of MADS-box genes in plants. Plant Mol Biol 42:115–149

    Article  PubMed  Google Scholar 

  • Theißen G, Becker A, Kirchner C, Münster T, Winter K-U, Saedler H (2002) How land plants learned their floral ABCs: the role of MADS-box genes in the evolutionary origin of flowers. In: Cronk QCB, Bateman RM, Hawkins JA (eds) Developmental genetics and plant evolution. Taylor & Francis, London, pp 173–205

    Google Scholar 

  • Vergara-Silva F (2003) Plants and the conceptual articulation of evolutionary developmental biology. Biol Philos 18:249–284

    Article  Google Scholar 

  • Wagner GP (2000) What is the promise of developmental evolution: part I: why is developmental biology necessary to explain evolutionary innovations? J Exp Zool (Mol Dev Evol) 288:95–98

    Article  CAS  Google Scholar 

  • Wagner GP, Laubichler MD (2004) Rupert Riedl and the re-synthesis of evolutionary and developmental biology: body plan and evolvability. J Exp Zool (Mol Dev Evol) 302B:92–102

    Article  Google Scholar 

  • Wagner GP, Müller GB (2002) Evolutionary innovations overcome ancestral constraints: a re-examination of character evolution in male sepsid flies (Diptera: Sepsidae). Evol Dev 4:1–6

    Article  PubMed  Google Scholar 

  • Wang R-L, Stec A, Hey J, Lukens L, Doebley J (1999) The limits of selection during maize domestication. Nature 398:236–239

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Nussbaum-Wagler T, Li B, Zhao Q, Vigouroux Y, Faller M, Bomblies K, Lukens L, Doebley JF (2005) The origin of the naked grains of maize. Nature 436:714–719

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

I thank Richard Bateman (London) and Jean Deutsch (Paris) for inspiring discussions about hopeful monsters, and Nicholas D. Holland (La Jolla) for bringing “some entertaining thoughts” on Crinoids to my attention. Many thanks also to Georgy Levit, Lennart Olsson and Olaf Breidbach (Jena) for their continuous interest in my views on the mechanisms of evolution. I am grateful to Lennart Olsson also for proofreading my manuscript. Work in my laboratory on the performance of a hopeful monster was supported by Grants TH417/4-1 and -2 from the Deutsche Forschungsgemeinschaft (DFG).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Günter Theißen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Theißen, G. Saltational evolution: hopeful monsters are here to stay. Theory Biosci. 128, 43–51 (2009). https://doi.org/10.1007/s12064-009-0058-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12064-009-0058-z

Keywords

Navigation