Journal Club, Sept. 18th: Genetic Drift, Founder Events, and Genetic Revolutions

Alan Templeton, Hamp Carson, Brian Charlesworth, and Nick Barton

By the early 1940s the importance of geographic isolation to speciation had been firmly established, and few have denied its important role since.  Although the geographic distributions of closely-related organisms rather clearly pointed to an important role for geographic isolation in speciation, it was not immediately clear from these distributional patterns what actually caused speciation.  Mayr and other architects of the synthesis discussed a wide range of hypothesizes mechanisms of speciation in the 1930s and 40s.

In 1954, however, Mayr began to advocate a mechanism for allopatric speciation that would strongly influence decades of subsequent work on speciation.  Marshaling evidence from nature – and from southeast Asian birds in particular – Mayr shows that widespread species on large islands are often relatively invariant while related populations isolated on smaller peripheral islands often exhibit extraordinary levels of phenotypic divergence.  To explain this pattern, Mayr developed a model for speciation involving isolation of small peripherally isolated populations that was inspired by population genetic studies of Fisher, Wright, Dobzhansky, and others.  In formulating this model, Mayr introduced several concepts that would strongly influence subsequent work on speciation, including the “co-adapted gene complex” and the idea that speciation tends to involve “genetic revolutions.”  Genetic revolutions involve a cascade of changes resulting from epistatic interactions among loci. Although Mayr never dismissed the important role that ecological variation and natural selection might play during founder events, he did argue that genetic revolutions in isolated populations are more important than selective differences experienced by populations connected by gene flow.

After Mayr proposed his admittedly “speculative” model involving genetic revolutions in peripherally isolated populations (later termed “peripatric speciation” [Mayr 1982]) several decades would pass before population geneticists developed more elaborate models to account for speciation resulting from genetic revolutions in founder populations.  In the late 1960s and early 1970s, the geneticist Hampton “Hamp” Carson developed his influential model of founder-flush speciation based on work with Hawaiian Drosophila.  Carson agreed with Mayr that adaptation via natural selection within a single geographically widespread population was insufficient for speciation, and that speciation was more likely accomplished by “a series of catastrophic, stochastic genetic events” that occur when small founder populations invade new territory.

Carson offered a very different explanation from Mayr’s to explain divergence of founder populations.  Most importantly, rejected Mayr’s assertion that founder populations diverge due to a dramatic reduction in genetic diversity; instead, Carson believed that founder populations tend to maintain rather high levels of genetic variation.  To Carson, however, this variation existed in the ancestral population as part of a “closed genetic system” that was not readily altered by selection or recombination under normal conditions because it was tied up in co-adapted gene complexes that were not readily altered without significant negative fitness consequences.  However, when selection was relaxed during a period of dramatic population growth associated with colonization of a new region – the flush period – recombination could break up coadapted gene complexes belonging to a species’ closed genetic variability system.  Although Carson viewed this release of genetic variation in a closed system as largely stochastic, his model was less reliant on genetic drift than Mayr’s because he believed that once variation was released it could in fact be very responsive to natural selection.   Influenced by Carson’s work, Templeton would later develop even more elaborate theories involving so-called genetic transilience.  By the mid-1980s these theories had gained considerable popularity and even played a central role in development of Eldgredge and Gould’s controversial theory of punctuated equilibrium.

By the early 1980s criticisms of founder event speciation via genetic revolution where emerging, led by papers by Charlesworth, Barton, Lande and others.(Charlesworth and Smith 1982, Charlesworth et al. 1982, Barton and Charlesworth 1984)  These papers ushered in the modern era of work on the genetics of speciation and resulted in an exchange between those who favored genetic revolutions and founder event speciation and those who favored gradual evolution of reproductive isolation in the pages of the Annual Review of Ecology and Evolutionary Biology (Barton and Charlesworth 1984, Carson and Templeton 1984).  The opponents of founder event speciation via founder-flush and transilience focused attention on core principles of population genetics and the lack of evidence for the type of genetic revolutions originally advanced by Mayr and later expanded and revised by Carson and Templeton.

This debate hardly marked the end of the controversy, which continued in the literature for more than a decade after this original exchange (Slatkin 1996, 1997, Charlesworth 1997, Gavrilets and Hasting 1996, Rundle et al. 1998, 1999, Templeton 1999).  Although founder events models are no longer widely discussed by population geneticists, Templeton remains a dedicated advocate for the role of founder events and transilience in speciation (Templeton 2008).

Readings are after the fold.

Required readings for Week 3:

Mayr, E. 1954. Change of Genetic and Environment in Evolution. Pages 157–180 in J. Huxley, A. C. Hardy, and E. B. Ford, editors. Evolution as a Process. Allen & Unwin, London.

Carson, H. L. 1975. The Genetics of Speciation at the Diploid Level. The American Naturalist 109:83–92.

Barton, N. H., and B. Charlesworth. 1984. Genetic revolutions, founder effects, and speciation. Annual Review of Ecology and Systematics 15:133–164.

Carson, H. L., and A. R. Templeton. 1984. Genetic revolutions in relation to speciation phenomena: the founding of new populations. Annual Review of Ecology and Systematics 15:97–131.

Background reading and reviews:

Mayr, E. 1982. The Growth of Biological Thought: Diversity, Evolution, and Inheritance. The Belknap Press of Harvard University Press. Cambridge, MA. (Pages 600-606 provide a nice overview of Mayr’s more recent thoughts on the role of founder events and genetic drift in speciation)

Coyne, J. A. and H. A. Orr. 2004. Speciation. Sinauer Associates, Inc. Sunderland, MA. (Chapter 11: “Selection versus Drift” and pages 105-111 in Chapter 3: “Allopatric and Parapatric Speciation”)

Coyne, J. A. 1994. Ernst Mayr and the origin of species. Evolution 48:19-30. (On the occassion of Mayr’s 100 birthday, Coyne’s paper reviews the history of founder event models and their challenges.  Coyne ultimately suggests that founder models have received undue attention relative to alternative “Darwinian” models.)

Templeton, A. R. 2004. Hampton Lawrence Carson 1914-2004: a biographical memoir. Pages 1–19. National Academy of Sciences, Washington, D. C. (In this extended obituary, Templeton recounts Carson’s contributions to founder models of speciation.)

Additional readings:

Baker, A. J., and A. Moeed. 1987. Rapid genetic differentiation and founder effect in colonizing populations of common mynas (Acridotheres tristis). Evolution:525–538.

Barton, N. H. 1996. Natural selection and random genetic drift as causes of evolution on islands. Philosophical Transactions Of The Royal Society B-Biological Sciences 351:785–795.

Barton, N. H., and B. Charlesworth. 1984. Genetic revolutions, founder effects, and speciation. Annual Review of Ecology and Systematics 15:133–164.

Boake, C. R. B., and S. Gavrilets. 1998. On the evolution of premating isolation after a founder event. American Naturalist 152:706–716.

Bryant, E. H., S. A. McCommas, and L. M. Combs. 1986. The effect of an experimental bottleneck upon quantitative genetic variation in the housefly. Genetics 114:1191–1211.

Carson, H. L. 1968. The population flush and its genetic consequences. Pages 123–137 in R. C. Lewontin, editor. Population Biology and Evolution. Syracuse University Press, Syracuse, NY.

Carson, H. L. 1970. Chromosome tracers of the origin of species. Science.

Carson, H. L. 1975. The genetics of speciation at the diploid level. The American Naturalist 109:83–92.

Carson, H. L. 1982. Evolution of Drosophila on the newer Hawaiian volcanoes. Heredity 48:3–25.

Carson, H. L. 1983. Chromosomal sequences and interisland colonizations in Hawaiian Drosophila. Genetics.

Carson, H. L., and A. R. Templeton. 1984. Genetic revolutions in relation to speciation phenomena: the founding of new populations. Annual Review of Ecology and Systematics 15:97–131.

Carson, H. L., and K. Y. Kaneshiro. 1976. Drosophila of Hawaii: systematics and ecological genetics. Annual Review of Ecology and Systematics 7:311–345.

Carson, H. L., and R. G. Wisotzkey. 1989. Increase in genetic variance following a population bottleneck. The American Naturalist 134:668–673.

Charlesworth, B. 1997. Is founder-flush speciation defensible? The American Naturalist 149:600–603.

Charlesworth, B., and D. B. Smith. 1982. A computer model of speciation by founder effects. Genetical Research 39:227–236.

Charlesworth, B., and S. Rouhani. 1988. The probability of peak shifts in a founder population. II. An additive polygenic trait. Evolution 42:1129–1145.

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

Clegg, S. M., S. M. Degnan, J. Kikkawa, C. Moritz, A. Estoup, and I. Owens. 2002. Genetic consequences of sequential founder events by an island-colonizing bird. Proceedings Of The National Academy Of Sciences Of The United States Of America 99:8127–8132.

Coulthart, M. B., L. R. Rhomberg, and R. S. Singh. 1984. The nature of genetic variation for species formation. Evolution 38:689–692.

Coyne, J. A. 1994. Ernst Mayr and the origin of species. Evolution 48:19–30.

Coyne, J. A., N. H. Barton, and M. Turelli. 2000. Is Wright’s shifting balance process important in evolution? Evolution 54:306–317.

Craddock, E. M., and W. E. Johnson. 1979. Genetic variation in Hawaiian Drosophila. V. chromosomal and allozymic diversity in Drosophila silvestris and its homosequential species. Evolution 33:137–155.

DeSalle, R., and A. R. Templeton. 1988. Founder effects and the rate of mitochondrial DNA evolution in Hawaiian Drosophila. Evolution 42:1076–1084.

DeSalle, R., and L. V. Giddings. 1986. Discordance of nuclear and mitochondrial DNA phylogenies in Hawaiian Drosophila. Proceedings of the National ….

Dobzhansky, T. 1972. Species of Drosophila. Science 177:664–669.

Florin, A. B., and A. Odeen. 2002. Laboratory environments are not conducive for allopatric speciation. Journal of Evolutionary Biology 15:10–19.

Galiana, A., A. Moya, and F. J. Ayala. 1993. Founder-flush speciation in Drosophila pseudoobscura: a large-scale experiment. Evolution 47:432–444.

Gavrilets, S., and A. Hastings. 1996. Founder effect speciation: a theoretical reassessment. The American Naturalist 147:466–491.

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

Goodnight, C. J. 1988. Epistasis and the effect of founder events on the additive genetic variance. Evolution 42:441–454.

Gould, S. J. 1980. Is a new and general theory of evolution emerging? Paleobiology:119–130.

Grant, P. R. 2002. Founder effects and silvereyes. Proceedings Of The National Academy Of Sciences Of The United States Of America 99:7818–7820.

Carson, H. L., F. E. Clayton, H. D. Stalker. 1967. Karyotypic stability and speciation in Hawaiian Drosophila. Proceedings Of The National Academy Of Sciences Of The United States Of America 57:1280.

Hare, M. P., F. Cipriano, and S. R. Palumbi. 2002. Genetic evidence on the demography of speciation in allopatric dolphin species. Evolution 56:804–816.

Harrison, R. G. 1991. Molecular changes at speciation. Annual Review of Ecology and Systematics 22:281–308.

Kambysellis, M. P., K.-F. Ho, E. M. Craddock, F. Piano, M. Parisi, and J. Cohen. 1995. Pattern of ecological shifts in the diversification of Hawaiian Drosophila inferred from a molecular phylogeny. Current Biology 5:1129–1139.

Kaneshiro, K. Y. 1980. Sexual isolation, speciation and the direction of evolution. Evolution:437–444.

Kaneshiro, K. Y. 1988. Speciation in the Hawaiian Drosophila: sexual selection appears to play an important role. Bioscience 38:258–263.

Lande, R. 1980. Genetic variation and phenotypic evolution during allopatric speciation. The American Naturalist 116:463–479.

Losos, J. B., T. W. Schoener, K. I. Warheit, and D. Creer. 2002. Experimental studies of adaptive differentiation in Bahamian Anolis lizards. Microevolution Rate, Pattern, Process:399–415.

Matioli, S. R., and A. R. Templeton. 1999. Coadapted gene complexes for morphological traits in Drosophila mercatorum. Two-loci interactions. Heredity 83:54–61.

Mayr, E. 1954. Change of genetic and environment in evolution. Pages 157–180 in J. Huxley, A. C. Hardy, and E. B. Ford, editors. Evolution as a Process. Allen & Unwin, London.

Mayr, E. 1982. Speciation and macroevolution. Evolution 36:1119–1132.

Moya, A., A. Galiana, and F. J. Ayala. 1995. Founder-effect speciation theory: failure of experimental corroboration. Proceedings of the National ….

Ohta, A. T. 1980. Coadaptive gene complexes in incipient species of Hawaiian Drosophila. The American Naturalist 115:121–132.

Powell, J. R. 1978. The founder-flush speciation theory: an experimental approach. Evolution 32:465–474.

Regan, J. L., L. M. Meffert, and E. H. Bryant. 2003. A direct experimental test of founder-flush effects on the evolutionary potential for assortative mating. Journal of Evolutionary Biology 16:302–312.

Rice, W. R., and E. E. Hostert. 1993. Laboratory experiments on speciation: what have we learned in 40 years? Ecography 47:1637.

Ringo, J. M. 1977. Why 300 species of Hawaiian Drosophila? The sexual selection hypothesis. Evolution 31:694–696.

Rouhani, S., and N. H. Barton. 1987. The probability of peak shifts in a founder population. Journal of Theoretical Biology 126:51–62.

Rundle, H. D. 2003. Divergent environments and population bottlenecks fail to generate premating isolation in Drosophila pseudoobscura. Evolution 57:2557–2565.

Rundle, H. D., A. O. Mooers, and M. C. Whitlock. 1998. Single founder-flush events and the evolution of reproductive isolation. Evolution 52:1850–1855.

Rundle, H. D., A. O. Mooers, and M. C. Whitlock. 1999. Experimental tests of founder-flush: a reply to Templeton. Evolution 53:1632–1633.

Slatkin, M. 1996. In defense of founder-flush theories of speciation. American Naturalist 147:493–505.

Slatkin, M. 1997. Reply to Charlesworth. American Naturalist 149:604–605.

Templeton, A. R. 1979a. Once again, why 300 species of Hawaiian Drosophila? Evolution 33:513–517.

Templeton, A. R. 1979b. The unit of selection in Drosophila mercantorum. II. Genetic revolution and the origin of coadapted genomes in parthenogenetic strains. Genetics 92:1265–1282.

Templeton, A. R. 1980. The theory of speciation via the founder principle. Genetics 94:1011–1038.

Templeton, A. R. 1981. Mechanisms of speciation–a population genetic approach. Annual Review of Ecology and Systematics 12:23–48.

Templeton, A. R. 1996. Experimental evidence for the genetic-transilience model of speciation. Evolution 50:909–915.

Templeton, A. R. 1999. Experimental tests of genetic transilience. Evolution 53:1628–1632.

Templeton, A. R. 2004. Hampton Lawrence Carson 1914-2004: a biographical memoir. Pages 1–19. National Academy of Sciences, Washington, D. C.

Templeton, A. R. 2008. The reality and importance of founder speciation in evolution. BioEssays 30:470–479.

Wasserman, M. 1990. Review: New ideas on new species. Bioscience 40:788.

Weinberg, J. R., V. R. Starczak, and D. Jörg. 1992. Evidence for rapid speciation following a founder event in the laboratory. Evolution 46:1214–1220.

Whitlock, M. C. 1997. Founder effects and peak shifts without genetic drift: adaptive peak shifts occur easily when environments fluctuate slightly. Evolution 51:1044–1048.

Whitlock, M. C., and M. J. Wade. 1995. Speciation: founder events and their effects on X-linked and autosomal genes. The American Naturalist 145:676–685.

Wool, D. 1987. Differentiation of island populations: a laboratory model. The American Naturalist 129:188–202.