Abstract
Theories for the evolutionary advantages and disadvantages of sex address two fundamentally different questions: (i) Why does the genome of sexual lineages not “congeal,” (i.e., move toward a lowered recombination rate)?, and (ii) When there is a mixture of reproductively isolated clonal and sexual lineages, why do the clonals not accumulate and lead to a predominance of asexual reproduction within a clade? Here, we focus on the latter question. The relevant theory in this case is necessarily based on a special form of “lineage” selection between sexuals and clonals that do not share a common gene pool. We first briefly review the major genetic costs and benefits of clonal reproduction and conclude that the extant assemblage of theories provides an essentially complete description of the phenomenon. We next set out to combine and simplify these seemingly disparate theories by graphically representing the frameworks previously developed by Felsenstein (Genetics 78: 737–756, 1974) and Kimura and Maruyama (Genetics 54: 1337–1351, 1966) to show that the all of the proposed disadvantages to clonal reproduction can be expressed by a single factor: a decreased efficiency of natural selection in non-recombining lineages. This reduced efficiency derives from two distinct processes that only operate in clonal lineages: (i) background-trapping and (ii) the compensatory linkage disequilibrium that accrues in response to epistatic selection.
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Arnqvist G, Rowe L (2005). Sexual conflict. Princeton University Press, Princeton
Barton NH (1995) Linkage and the limits to natural selection. Genetics 140: 821–841
Bell G (1982) The masterpiece of nature: the evolution and genetics of sexuality. Croom Helm and University of California Press, London and Berkeley
Beerenwinkel N, Pachter L, Sturmfels B, Elena SF, Lenski RE (2007) Analysis of epistatic interactions and fitness landscapes using a new geometric approach. BMC Evol Biol 7: 60
Burt A (2000) Perspective: sex, recombination, and the efficacy of selection – was Weismann right? Evolution 54: 337–351
Burt A, Bell G, Harvey PH (1991) Sex differences in recombination. J Evol Biol 4: 259–277
Burt A, Trivers R (2006) Genes in conflict: the biology of selfish genetic elements. Belknap Press, Cambridge, MA
Butlin RK, Griffiths HI (1993) Ageing without sex? Nature 364: 680
Chapman T, Liddle LF, Kalb JM, Wolfner MF, Partridge L (1995) Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373: 241–244
Charlesworth B (1994) The effect of background selection against deleterious mutations on weakly selected, linked variants. Genet Res 63: 213–227
Clarke DK, Duarte EA, Elena SF, Moya A, Domingo E, Holland JJ (1994) The Red Queen reigns in the kingdom of RNA viruses. Proc Natl Acad Sci USA 91: 4821–4824
Crow JF, Kimura M (1970) An introduction to population genetic theory. Harper and Row, New York
Elena SF, Lenski RE (1997) Test of synergistic interactions among deleterious mutations in bacteria. Nature 390: 395–398
Eyre-Walker A, Woolfit M, Phelps T (2006) The distribution of fitness effects of new deleterious amino acid mutations in humans. Genetics 173: 891–900
Felsenstein J (1974) Evolutionary advantage of recombination. Genetics 78: 737–756
Fisher RA (1930) The genetical theory of natural selection. Oxford University Press, Oxford
Fowler K, Partridge L (1989) A cost of mating in female fruitflies. Nature 338: 760–761
Gerrish PJ, Lenski RE (1998) The fate of competing beneficial mutations in an asexual population. Genetica 102–103: 127–144
Haag-Liautard C, Dorris M, Maside X, Macaskill S, Halligan DL, Charlesworth B, Keightley PD (2007) Direct estimation of per nucleotide and genomic deleterious mutation rates in Drosophila. Nature 445: 82–85
Hamilton WD (1980) Sex versus non-sex versus parasite. Oikos 35: 282–290
Jaenike J (1978) A hypothesis to account for the maintenance of sex within populations. Evol Theory 3: 191–194
Keightley PD, Otto SP (2006) Interference among deleterious mutations favours sex and recombination in finite populations. Nature 443: 89–92
Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge, UK
Kimura M, Maruyama T (1966) Mutational load with epistatic gene interactions in fitness. Genetics 54: 1337–1351
Kondrashov AS (1988) Deleterious mutations and the evolution of sexual reproduction. Nature 336: 435–440
Kondrashov AS (1993) Classification of hypotheses on the advantage of amphimixis. J Hered 84: 372–387
Lattorff HMG, Moritz RFA, Fuchs S (2005) A single locus determines thelytokous parthenogenesis of laying honeybee workers (Apis mellifera capensis). Heredity 94: 533–537
Li W-H (1978) Maintenance of genetic variability under joint effect of mutation, selection and random drift. Genetics 90: 349–382
Lively CM, Lloyde DG (1990) The cost of biparental sex under individual selection. Am Nat 135: 489–500
Manning JT (1983) The consequences of mutation in multiclonal asexual species. Heredity 50: 15–19
Maynard Smith J (1978) The Evolution of sex. Cambridge University Press, Cambridge, UK
Muller HJ (1932) Some genetic aspects of sex. Am Nat 66: 118–138
Muller HJ (1964) The relation of recombination to mutational advance. Mutat Res 1: 2–9
Otto SP, Lenormand T (2002) Resolving the paradox of sex and recombination. Nat Rev Genet 3: 252–261
Parker GA (1979) Sexual selection and sexual conflict. In: Blum MS and Blum NA (eds) Sexual selection and reproductive competition in insects. Academic Press, New York, pp. 123–166
Peck JR (1994) A ruby in the rubbish: beneficial mutations, deleterious mutations and the evolution of sex. Genetics 137: 597–606
Rice WR (1983) Parent-offspring pathogen transmission: a selective agent promoting sexual recombination. Am Nat 121: 187–203
Rice WR (1987) Genetic hitch-hiking and the evolution of reduced genetic activity of the Y sex chromosome. Genetics 116: 161–167
Rice WR (1996a) Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 361: 232–234
Rice WR (1996b) Evolution of the Y sex chromosome in animals. BioScience 46: 331–343
Rice WR (1998) Requisite load, pathway epistasis, and deterministic mutation accumulation in sexual versus asexual populations. Genetica 102–103: 71–81
Rice WR, Chippindale AK (2001) Sexual recombination and the power of natural selection. Science 294: 555–559
Rice WR, Holland B (1997) The enemies within: intergenomic conflict, interlocus contest evolution (ICE), and the intraspecific Red Queen. Behav Ecol Sociobiol 41: 1–10
Rice WR, Linder JE,Friberg U, Lew TA, Morrow EH, Stewart AD (2005) Inter-locus antagonistic coevolution as an engine of speciation: assessment with hemiclonal analysis. Proc Natl Acad Sci USA 102 (Suppl. 1): 6527–6534
Rice WR, Stewart AD, Morrow EH, Linder JE, Orteiza N, Byrne PG (2006) Assessing sexual conflict in the Drosophila melanogaster laboratory model system. Philos Trans R Soc Biol 361: 287–299
Rowe L, Arnqvist G, Sih A, Krupa JJ (1994) Sexual conflict and the evolutionary ecology of mating patterns: water striders as a model system. Trends Ecol Evol 9: 289–293
Stebbins GL (1950) Variation and evolution in plants. Columbia University Press, New York
Van Valen L (1973) A new evolutionary law. Evol Theory 1: 1–30
Vijverberg K, Van der Hulst RGM, Lindhout P, Van Dijk PJ (2004) A genetic linkage map of the diplosporous chromosomal region in Taraxacum officinale (common dandelion; Asteraceae). Theor Appl Genet 108: 725–732
Welch DM, Meselson M (2000) Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 288: 1211–1215
Werren JH (1997) Biology of Wolbachia. Annu Rev Entomol 42: 587–609
West SA, Lively CM, Read AF (1999) A pluralist approach to sex and recombination. J Evol Biol 12: 1003–1012
Westwood MN (1993) Temperate-zone pomology, physiology and culture. Timber Press, Portland, Oregon
White MJD (1973) Animal cytology and evolution, 3rd ed. Cambridge University Press, Cambridge, UK
White MJD (1978) Modes of speciation. WH Freeman, San Francisco
Williams GC (1975) Sex and evolution. Princeton University Press, New Jersey
Acknowledgements
WRR was supported by grants from the National Science Foundation (DEB-0128780 and DEB-0111613) and UF by a stipend from Lennader’s foundation and a fellowship from the Wenner-Gren Foundations. We thank K. Schoenrock for comments on the manuscript.
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Rice, W.R., Friberg, U. (2009). A Graphical Approach to Lineage Selection Between Clonals and Sexuals. In: Schön, I., Martens, K., Dijk, P. (eds) Lost Sex. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-2770-2_5
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DOI: https://doi.org/10.1007/978-90-481-2770-2_5
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