Skip to main content
Springer Nature Link
Log in

Toward a new synthesis: population genetics and evolutionary developmental biology

  • Published:
Save article
View saved research
Genetica Aims and scope Submit manuscript

Abstract

Despite the recent synthesis of developmental genetics and evolutionary biology, current theories of adaptation are still strictly phenomenological and do not yet consider the implications of how phenotypes are constructed from genotypes. Given the ubiquity of regulatory genetic pathways in developmental processes, we contend that study of the population genetics of these pathways should become a major research program. We discuss the role divergence in regulatory developmental genetic pathways may play in speciation, focusing on our theoretical and computational investigations. We also discuss the population genetics of molecular co-option, arguing that mutations of large effect are not needed for co-option. We offer a prospectus for future research, arguing for a new synthesis of the population genetics of development.

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

Access this article

Log in via an institution

Subscribe and save

Springer+
from €39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Explore related subjects

Discover the latest articles, books and news in related subjects, suggested using machine learning.

References

  • Arnold, S.J., 1983. Morphology, performance, and fitness. Am. Zool. 23: 347–361.

    Google Scholar 

  • Arnold, S.J., M.E. Pfrender & A.G. Jones, 2001. The adaptive landscape as a conceptual bridge between microevolution and macroevolution. Genetica 112-113: 9–32.

    Google Scholar 

  • Arnold, S.J. & P.C. Phillips, 1999. Hierarchical comparison of genetic variance-covariance matrices. II. Coastal-inland divergence in the garter snake, Thamnophis elegans. Evolution 53: 1516–1527.

    Google Scholar 

  • Arnone, M.I. & E.H. Davidson, 1997. The hardwiring of development: organization and function of genomic regulatory elements. Development 124: 1851–1864.

    Google Scholar 

  • Barton, N.H. & M. Turelli, 1989. Evolutionary quantitative genetics: How little do we know? Ann. Rev. Genet. 23: 337–370.

    Google Scholar 

  • Bender, W., M. Akjam, F. Karch, P.A. Beachy, M. Peifer, P. Spierer, E.B. Lewis & D.S. Hogness, 1983. Molecular genetics of the bithorax complex in D. melanogaster. Science 221: 23–29.

    Google Scholar 

  • Boguski, M.S., 1999. Biosequence exegesis. Science 286: 453–455.

    Google Scholar 

  • Bradshaw, H.D., Jr., K.G. Otto, B.E. Frewen, J.K. McKay & D.W. Schemske, 1998. Quantitative trait loci affecting differences in floral morphology between two species of monkeyflower (Mimulus). Genetics 149: 367–382.

    Google Scholar 

  • Bryant, E.H., S.A. McCommas & L.M. Coombs, 1986. The effect of an experimental bottleneck upon quantitative genetic variation in the housefly. Genetics 114: 1191–1223.

    Google Scholar 

  • Charkesworth, B., R. Lande & M. Slatkin, 1982. A neo-Darwinian commentary on macroevolution. Evolution 36: 474–498.

    Google Scholar 

  • Cohen, F.M., 1984. Genetic divergence under uniform selection. I. Similarity among populations of Drosophila melanogaster in their responses to artificial selection for modifiers of ciD. Evolution 38: 55–71.

    Google Scholar 

  • Conway Morris, S., 2000. Evolution: bringing molecules into the fold. Cell 100: 1–11.

    Google Scholar 

  • Coyne, J.A., 1992. Genetics and speciation. Nature 355: 511–515.

    Google Scholar 

  • Coyne, J.A., 1995. Speciation in monkeyflowers. Nature 376: 726–727.

    Google Scholar 

  • Darwin, C., 1859. On the Origin of Species. John Murray, London.

  • Davidson, E.H., 1986. Gene Activity in Early Development. Academic Press, San Diego, 3rd edn.

    Google Scholar 

  • Dobzhansky, Th., 1937. Genetics and the Origin of Species. Columbia University Press, New York.

    Google Scholar 

  • Ephrussi, B., 1958. The Cytoplasm and Somatic Cell Variation. J. Cell. Compar. Physiol. 52 (suppl.): 35–54.

    Google Scholar 

  • Falconer, D.S. & T.F.C MacKay, 1996. Introduction to Quantitative Genetics. Longman, Harlow, U. K., 4th edn.

  • Feder, J.L., 1998. The Apple Maggot fly, Rhagoletis pomonella: flies in the face of conventional wisdom about speciation?, pp. 130–144 in Endless Forms: Species and Speciation, edited by D.J. Howard & S.H. Berlocher. Oxford University Press, New York.

    Google Scholar 

  • Feder, M.E. & W.B. Watt, 1992. Functional biology of adaptation, pp. 365–392 in Genes in Ecology, edited by R. J. Berry, T. J. Crawford & G.M. Hewitt. Blackwell Scientific Publications, Oxford.

    Google Scholar 

  • Felsenstein, J., 1985. Phylogenies and the comparative method. Amer. Natur. 125: 1–15.

    Google Scholar 

  • Fields, S., 2001. Proteomics - proteomics in genomeland. Science 291: 1221.

    Google Scholar 

  • Fisher, R.A., 1930. The Geneticial Theory of Natural Selection. Dover Press, New York.

    Google Scholar 

  • Frank, S.A., 1999. Population and quantitative genetics of regulatory networks. J. Theor. Biol. 197: 281–294.

    Google Scholar 

  • Futuyma, D. J., 1998. Evolutionary Biology. Sinauer Associates, Sunderland, M.A., 3rd edn.

    Google Scholar 

  • Garstang, W., 1922. The theory of recapitulation: a critical restatement of the biogenetic law. J. Linn. Soc. Zool. 35: 81–101.

    Google Scholar 

  • Gavrilets, S., 1997. Evolution and speciation on holey adaptive landscapes. Trends Ecol. Evol. 12: 307–312.

    Google Scholar 

  • Gavrilets, S., 1999. A dynamical theory of speciation on holey adaptive landscapes. Amer. Natur. 154: 1–22.

    Google Scholar 

  • Gavrilets, S., H. Li & M.D. Vose, 2000. Patterns of parapatric speciation. Evolution 54: 1126–1134.

    Google Scholar 

  • Gerhart, J. & M. Kirschner, 1997. Cells, Embryos, and Evolution. Blackwell Science.

  • Gibson, G., 1996. Epistasis and pleiotropy as natural properties of transcriptional regulation.Theor. Pop. Biol. 49: 58–89.

    Google Scholar 

  • Gilbert, S.F., 1988. pp. 311–346. in The American Development of Biology, edited by R. Rainger, K.R. Benson & J. Maienschein. University of Pennsylvania Press, Philadelphia, P.A.

    Google Scholar 

  • Gilbert, S.F., 1997. Developmental Biology. Sinauer Press, Sunderland, M.A., 5th edn.

    Google Scholar 

  • Gilbert, S.F., 2000. Genes classical and genes developmental: the different uses of the gene in evolutionary syntheses, pp. 178–192 in The Concept of the Gene in Development and Evolution, edited by P. Buerton, R. Falk & H.-J. Rheinberger. Cambridge University Press, Cambridge, U.K.

    Google Scholar 

  • Gilbert, S.F., J.M. Opitz & R.A. Raff, 1996. Resynthesizing evolutionary and developmental biology. Devel. Biol. 173: 357–372.

    Google Scholar 

  • Goldschmidt, R., 1940. The Material Basis of Evolution. Yale University Press, New Haven, C.T.

    Google Scholar 

  • Goodnight, C.J., 1987. On the effect of founder events on epistatic genetic variance. Evolution 41: 80–91.

    Google Scholar 

  • Gromko, M.H., 1995. Unpredictability of correlated response to selection - pleiotropy and sampling interact. Evolution 49: 685–693.

    Google Scholar 

  • Halder, G., P. Callaerts & W.J. Gehring, 1995. Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267: 1788–1792.

    Google Scholar 

  • Hansen, T.F. & G.P. Wagner, 2001. Modeling genetic architecture: a multilinear theory of gene interaction. Theor. Pop. Bio. 59: 61–86.

    Google Scholar 

  • Hendry, A., J.K. Wenburg, P. Bentzen, E.C. Volk & T.P. Quinn, 2000. Rapid evolution of reproductive isolation in the wild: evidence from introduced salmon. Science 290: 516–518.

    Google Scholar 

  • Hey, J. & R.M. Kliman, 1993. Population genetics and phylogenetics of DNA sequence variation at multiple loci within the Drosophila melanogaster species complex. Mol. Biol. Evol. 10: 804–822.

    Google Scholar 

  • Hillis, D.M., C. Moritz & B. Mable, 1996. Molecular Systematics. Sinauer Associates, Sunderland, M.A., 2nd edn.

    Google Scholar 

  • Johnson, N.A., 1998. Postzygotic reproductive isolation: epigenetics for an epiphenomenon? J. Evol. Biol. 11: 207–212.

    Google Scholar 

  • Johnson, N.A., 2000a. Gene interaction and the origin of species, pp. 197–212 in Epistasis and the Evolutionary Process, edited by J.B. Wolf, E.D. Brodie III & M.J. Wade. Oxford University Press, New York.

    Google Scholar 

  • Johnson, N.A., 2000b. Speciation: Dobzhansky-Muller incompatibilities, dominance, and gene interaction. Trends Ecol. Evol. 15: 480–482.

    Google Scholar 

  • Johnson, N.A. & A.H. Porter, 2000. Rapid speciation via parallel, directional selection on regulatory genetic pathways. J. Theor. Biol. 205: 527–542.

    Google Scholar 

  • Johnson, N.A. & M.J. Wade, 1996. Genetic covariances within and between species: indirect selection for hybrid inviability. J. Evol. Biol. 9: 205–214.

    Google Scholar 

  • Jones, S., 1999. Darwin' Ghost: ‘The Origin of Species’ Updated. Ballantine, New York.

  • Kauffman, S., 1993. The Origins of Order: Self-Organization and selection in Evolution. Oxford University Press, New York.

    Google Scholar 

  • Kliman, R.M., P. Andolfatto, J.A. Coyne, F. Depaulis, M. Kreitman, A.J. Berry, J. McCarter, J. Wakeley & J. Hey, 2000. The population genetics of the origin and divergence of the Drosophila simulans complex species. Genetics 156: 1913–1931.

    Google Scholar 

  • Kohler, R.E., 1994. Lords of the Fly: Drosophila Genetics and Experimental Life. University of Chicago Press, Chicago.

    Google Scholar 

  • Lascoux, M., 1997. Unpredictability of correlated response to selection: linkage and initial frequency also matter. Evolution 51: 1394–1400.

    Google Scholar 

  • Lewin, B., 1997. Genes VI. Oxford University Press, Oxford.

    Google Scholar 

  • Lewis, E.B., 1978. A gene complex controlling segmentation in Drosophila. Nature 276: 565–570.

    Google Scholar 

  • Lewontin, R.C., 1974. The Genetic Basis of Evolutionary Change. Harvard University Press.

  • Losos, J.B., T.R. Jackman, A. Larson, K. de Queiroz & L. Rodriguez-Schettino, 1998. Contingency and determinism in replicated adaptive radiations of island lizards. Science 279: 2115–2118.

    Google Scholar 

  • Ludwig, M.Z., C. Bergman, N.H. Patel & M. Kreitman, 2000. Evidence for stabilizing selection in a eukaryotic enhancer element. Nature 403: 564–567.

    Google Scholar 

  • Lyman, R.F. & T.F.C. MacKay, 1998. Candidate quantitative trait loci and naturally occurring phenotypic variation for bristle number in Drosophila melanogaster: the Delta-Hairless gene region.

  • Lynch, M. & A.G. Force, 2000. The origin of interspecific genomic incompatibility via gene duplication. Amer. Natur. 156: 590–605.

    Google Scholar 

  • Lynch, M. & J.B. Walsh, 1998. Fundamentals of Quantitative Genetics. Sinauer Associates, Sunderland, M.A.

    Google Scholar 

  • Mackay, T.F.C., 1995. The genetic basis of quantitative variation: numbers of sensory bristles of Drosophila melanogaster as a model system. Trends Genet. 11: 464–470.

    Google Scholar 

  • Mackay, T.F.C., 1996. The nature of quantitative genetic variation revisited: lessons from Drosophila bristles. BioEssays 18: 113–121.

    Google Scholar 

  • MacKay, T.F.C. & C.H. Langley, 1990. Molecular and phenotypic variation in the achaete-scute region of Drosophila melanogaster. Nature 348: 64–66.

    Google Scholar 

  • Martins, E.P. (ed.), 1996. Phylogenies and the Comparative Method in Animal Behavior. Oxford University Press, New York.

    Google Scholar 

  • Mayr, E., 1963. Animal Species and Evolution. Harvard University Press, Cambridge, M.A.

    Google Scholar 

  • Mayr, E., 1982. The Growth of Biological Thought. Harvard University Press, Cambridge, M.A.

    Google Scholar 

  • McGinnis, W.C., R.L. Garber, J. Wirz, A. Kurioiwa & W.J. Gehring, 1984a. A homologous protein-coding sequence in Drosophila homeotic genes and its conservation in other metazoans. Cell 37: 403–408.

    Google Scholar 

  • McGinnis, W., M.S. Levine, E. Hafen, A. Kuroiwa & W. Gehring, 1984b. A conserved DNA sequence in homeotic genes of the Drosophila antennapedia and Bithorax complexes. Nature 308: 428–433.

    Google Scholar 

  • McPeek, M., 1995. Testing hypotheses about evolutionary change on single branches of a phylogeny using evolutionary contrasts. Am. Nat. 145: 686–703.

    Google Scholar 

  • Muller, H.J., 1942. Isolating mechanisms, speciation, and temperature. Biol. Symp. 6: 71–125.

    Google Scholar 

  • Munn, J.S. & R. Kopan, 2000. Notch signaling: from the outside in. Devel. Biol. 228: 151–165.

    Google Scholar 

  • Nagy, L., 1998. Changing patterns of gene regulation in the evolution of arthropod morphology. Amer. Zool. 38: 818–828.

    Google Scholar 

  • Nanney, D.L., 1982. Genes and phenes in Tetrahymena. Bioscience 783–788.

  • Nusselin-Volhard, C. & E. Wieschaus, 1980. Mutations affecting segmentation number and polarity in Drosophila. Nature 287: 795–801.

    Google Scholar 

  • Orr, H.A., 1995. The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics 139: 1805–1813.

    Google Scholar 

  • Orr, H.A., 1998. The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52: 935–949.

    Google Scholar 

  • Orr, H.A., L.D. Madden, J.A. Coyne, R. Goodwin & R.S. Hawley, 1997. The developmental basis of hybrid inviability: a mitotic defect in Drosophila hybrids. Genetics 145: 1031–1040.

    Google Scholar 

  • Orr, H.A. & J.A. Coyne, 1992. The genetics of adaptation: a reassessment. Amer. Natur. 140: 725–742.

    Google Scholar 

  • Palopoli, M.F. & N.H. Patel, 1996. Neo-Darwinian developmental evolution: can we bride the gap between pattern and process? Curr. Opin. Genet. Devel. 6: 502–508.

    Google Scholar 

  • Pederson, J.A., J.W. La Follette, C. Gross, A. Veraksa, W. McGinnis & J.W. Mahaffey, 2000. Regulation by homeoproteins: a comparsion of deformed-responsive elements. Genetics 156: 677–686.

    Google Scholar 

  • Perez, D.E., 1994. Genetics of postmating reproductive isolation in Drosophila: investigation of an X-linked hybrid sterility region. PhD Dissertation, University of Chicago, Chicago, I.L.

    Google Scholar 

  • Perez, D.E. & C.-I. Wu, 1995. Further characterization of the Odysseus locus of hybrid sterility in Drosophila: one gene is not enough. Genetics 140: 201–206.

    Google Scholar 

  • Perez, D.E., C.-I. Wu, N.A. Johnson & M.-L. Wu, 1993. Genetics of reproductive isolation in the Drosophila simulans clade: DNA marker-assisted mapping of a hybrid-male sterility gene, Odysseus (Ods). Genetics 134: 261–275.

    Google Scholar 

  • Phillips, P.C., 1999. From complex traits to complex alleles. Trends Genet. 15: 6–8.

    Google Scholar 

  • Phillips, P.C. & S.J. Arnold, 1999. Hierarchical comparison of genetic variance-covariance matrices. I. Using the Flury hierarchy. Evolution 53: 1506–1515.

    Google Scholar 

  • Phillips, P.C., M.C. Whitlock & K. Fowler, 2001. Inbreeding changes the shape of the genetic covariance matrix in Drosophila melanogaster. Genetics (in review).

  • Pigliucci, M. & C.D. Schlichting, 1997. On the limits of quantitative genetics for the study of phenotypic evolution. Acta Biotheor. 45: 143–160.

    Google Scholar 

  • Pray, L.A. & C.J. Goodnight, 1995. Genetic variability in inbreeding depression in the flour beetle, T. castaneum. Evolution 49: 176–188.

    Google Scholar 

  • Quiring, R., U. Walldorf, U. Kloter & W.J. Gehring, 1994. Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Anirida in humans. Science 265: 785–789.

    Google Scholar 

  • Raff, R.C., 1996. The Shape of Life. University of Chicago Press, Chicago.

    Google Scholar 

  • Rice, S.H., 1998. The evolution of canalization and the breaking of von Baer' laws: modeling the evolution of development with epistasis. Evolution 52: 647–656.

    Google Scholar 

  • Rice, S.H., 2000. The evloution of developmental interactions, pp. 82–98 in Epistasis and the Evolutionary Process, edited by J.B. Wolf, E.D. Brodie III & M.J. Wade. Oxford University Press, New York.

    Google Scholar 

  • Roff, D.A., 2000. The evolution of the G matrix: selection or drift? Heredity 84: 135–142.

    Google Scholar 

  • Roff, D.A. & T.A. Mousseau, 1999. Does natural selection alter genetic architecture? An evaluation of quantitative genetic variation among populations of Allonemobius socius and A. fasciatus. J. Evol. Biol. 12: 361–369.

    Google Scholar 

  • Rundle, H.D. & M.C. Whitlock, 2001. A genetic interpretation of ecologically dependent isolation. Evolution 55: 198–201.

    Google Scholar 

  • Sawamura, K., A.W. Davis & C.-I. Wu, 2000. Genetic analysis of speciation by means of introgression into Drosophila melanogaster. Proc. Nat. Acad. Sci. U.S.A. 97: 2652–2655.

    Google Scholar 

  • Schemske, D.W. & H.D. Bradshaw, Jr., 1999. Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). Proc. Natl. Acad. Sci. U.S.A. 96: 11910–11915.

    Google Scholar 

  • Schulter, D., 1998. Ecological causes of speciation, pp. 114–129 in Endless Forms: Species and Speciation, edited by D.J. Howard and S.H. Berlocher. Oxford University Press, New York.

    Google Scholar 

  • Schulter, D., 2000. The Ecology of Adaptive Radiation. Oxford University Press, New York.

    Google Scholar 

  • Schutt, C. & R. Nothiger, 2000. Structure, function, and evolution of sex-determining systems in Dipeteran insects. Development 127: 667–677.

    Google Scholar 

  • Scott, M.P. & A.J. Weiner, 1984. Structural relationships among genes that control development: sequence homology between the Antennapedia, Ultrabithroax, and fushi tarazu loci of Drosophila. Proc. Natl. Acad. Sci. U.S.A. 81: 4115–4119.

    Google Scholar 

  • Skaer, N. & P. Simpson, 2000. Genetic analysis of bristle loss in hybrids between Drosophila melanogaster and D. simulans provides evidence for divergence of cis-regulatory sequences in the achaete-scute gene complex. Devel. Biol. 221: 148–167.

    Google Scholar 

  • Stern, D., 2000. Perspective: evolutionary developmental biology and the problem of variation. Evolution 54: 1079–1091.

    Google Scholar 

  • Sucena, E. & D.L. Stern, 2000. Divergence of larval morphology between Drosophila sechellia and its sibling species caused by cis-regulatory evolution of ovo/shaven-baby. Proc. Natl. Acad. Sci. U.S.A. 97: 4530–4534.

    Google Scholar 

  • Templeton, A.R., 1981. Mechanisms of speciation - a population genetic approach. Ann. Rev. Ecol. Syst. 12: 23–48.

    Google Scholar 

  • Thompson, D.W., 1942. On Growth and Form. Cambridge University Press, Cambridge, U.K.

    Google Scholar 

  • Ting, C.-T., S.-C. Tsaur, M.-L. Wu & C.-I. Wu, 1998. A rapidly evolving homeobox at the site of a hybrid sterility gene. Science 282: 1501–1504.

    Google Scholar 

  • Ting, C.T., S.C. Tsaur & C.-I. Wu, 2000. The phylogeny of closely related species as revealed by the genealogy of a speciation gene, Odysseus. Proc. Natl. Acad. Sci. U.S.A. 97: 5313–5316.

    Google Scholar 

  • Turelli, M. & H.A. Orr, 2000. Dominance, epistasis, and the genetics of postzygotic isolation. Genetics 154, 1663–1679.

    Google Scholar 

  • Wade, M.J., 2000. pp. 213–231 in Epistasis and the Evolutionary Process, edited by J.B. Wolf, E.D. Brodie III & M.J. Wade. Oxford University Press, New York.

    Google Scholar 

  • Wagner, G.P., 1996. Does evolutionary plasticity evolve? Evolution 50: 1008–1023.

    Google Scholar 

  • Wake, D.B., G. Roth & M. Wake, 1983. On the problem of stasis in organismal evolution. J. Theor. Biol. 101: 211–224.

    Google Scholar 

  • Wolf, J.B., W.A. Frankino, A.F. Agrawal, E.D. Brodie III & A.J. Moore, 2001. Developmental interactions and the constituents of quantitative variation. Evolution 55: 232–245.

    Google Scholar 

  • Wright, S., 1968. Evolution and the Genetics of Populations. Vol. I., Genetic and Biometric Foundations. University of Chicago Press, Chicago.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Entomology and Program in Organismic and Evolutionary Biology, University of Massachusetts, 102 Fernald Hall, Amherst, MA, 01003, USA

    Norman A. Johnson & Adam H. Porter

Authors
  1. Norman A. Johnson
    View author publications

    Search author on:PubMed Google Scholar

  2. Adam H. Porter
    View author publications

    Search author on:PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Johnson, N.A., Porter, A.H. Toward a new synthesis: population genetics and evolutionary developmental biology. Genetica 112, 45–58 (2001). https://doi.org/10.1023/A:1013371201773

Download citation

  • Issue date:

  • DOI: https://doi.org/10.1023/A:1013371201773