Mutation Load and the Survival of Small Populations

Abstract

Abstract. -Previous attempts to model the joint action of selection and mutation in finite populations have treated population size as being independent of the mutation load. However, the accumulation of deleterious mutations is expected to cause a gradual reduction in population size. Consequently, in small populations random genetic drift will progressively overpower selection making it easier to fix future mutations. This synergistic interaction, which we refer to as a mutational melt-down, ultimately leads to population extinction. For many conditions, the coefficient of variation of extinction time is less than 0.1, and for species that reproduce by binary fission, the expected extinction time is quite insensitive to population carrying capacity. These results are consistent with observations that many cultures of ciliated protozoans and vertebrate fibroblasts have characteristic extinction times. The model also predicts that c10nallineages are unlikely to survive more than 10 4 to 10' generations, which is consistent with existing data on parthenogenetic animals. Contrary to the usual view that Muller's ratchet does more damage when selection is weak, we show that the mean extinction time declines as mutations become more deleterious. Although very small sexual populations, such as self-fertilized lines, are subject to mutational meltdowns, recombination effectively eliminates the process when the effective population size exceeds a dozen or so. The concept ofthe effective mutation load is developed, and several procedures for estimating it are described. It is shown that this load can be reduced substantially when mutational effects are highly variable.Received June 27, 1989. Accepted January 17, 1990.All populations are doomed to eventual in small populations. On the other hand, extinction. The reasons include temporal Kimura et al. (1963) argued that the load variation in the environment, demographic due to mildly deleterious mutations is instochasticity (random variation in survi-versely proportional to population size, apvorship, birth rate, and sex ratio), and ge-proaching the selection coefficient in the abnetic problems such as inbreeding depres-sence of back-mutation. sion, the loss of adaptive variation by These results for sexual populations in random drift, and recurrent deleterious mu-drift-mutation-selection balance may be tations (Soule, 1987;Lande, 1988). This pa-contrasted with Muller's (1964) idea that a per is concemed exclusively with the latter mutational ratchet operates in asexual popproblem. Deleterious mutations impose a ulations, continually driving them to lower load on populations through the reduction and lower fitness. The idea here is that, in in the mean survivorship and/or reproduc-the absence of sex, no genotype can ever tive rates of individuals (Haldane, 1937; produce an offspring with fewer mutations Muller, 1950;Wallace, 1987). IDtimately, than its own load. In a finite population, this load should be manifested in a higher there is always a possibility that the class ...

How populations persist when asexuality requires sex: the spatial dynamics of coping with sperm parasites

“…Sexual species suffer from the twofold cost of sex, which implies that they should be quickly outcompeted by asexual forms that use the same resources but can produce eggs at twice the rate (Williams 1975;Maynard Smith 1978;Agrawal 2001Agrawal , 2006. On the other hand, asexual reproduction appears to be associated with long-term costs such as deleterious mutation accumulation (Muller 1964;Kondrashov 1988;Lynch & Gabriel 1990) and limited ability to adapt to changing environmental conditions (Bell 1982;Waxman & Peck 1999) or higher vulnerability to parasites (reviewed in Hamilton et al 1990). Asexual lineages are therefore typically fairly short-lived (e.g.…”

“…Asexual lineages are therefore typically fairly short-lived (e.g. Muller 1964;Lynch & Gabriel 1990;Lynch et al 1993;Crow 1994;Dunbrack et al 1995; but see ancient asexuals: Judson & Normark (1996)). Indeed, much of the literature on the evolution of sex attempts to weigh the short-term advantage of the twofold benefit of asexual reproduction with the long-term benefits of sex, as well as asking whether sex has significant benefits that act already over shorter time-scales (e.g.…”

Accumulation of Deleterious Mutations in Small Abiotic Populations of RNA

“…Another issue of great interest is the relationship between mutational load and population size. It has been predicted that these two factors can act synergistically, in that as the load increases, the population size should decrease, leading to a higher probability of fixing new deleterious mutations (Lynch and Gabriel 1990;Gabriel et al 1993;Lynch et al 1993). Eventually a threshold is crossed, and the population spirals into extinction via a ''mutational meltdown,'' as can be seen in ciliated protozoans and fibroblast cultures, for example (Smith and Pereira-Smith 1977;Tagaki and Yoshida 1980).…”

The Mutational Meltdown in Asexual Populations

“…This phenomenon, now known as Muller's ratchet (Felsenstein 1974), has been subject to numerous theoretical studies with the objective of evaluating the rate at which mean population fitness decays under asexuality (Bell 1988a,b;Birky and Walsh 1988;Charlesworth 1990;Gabriel et al, in press;Haigh 1978;Kondrashov 1982Kondrashov , 1984Lynch and Gabriel 1990;Maynard Smith 1978;Melzer and Koeslag 1991;Pamilo et al 1987). But with few exceptions (Bell 1988a,b;Gabriel et al, in press;Lynch and Gabriel 1990;Melzer and Koeslag 1991), these studies have been pursued under the assumption that population size is unaffected by the accumulation of mutations.…”

“…Although data are available for only a small number of species (Bell 1988b;Charlesworth et al 1990;Crow and Simmons 1983;Houle et al 1992;Lynch and Gabriel 1990;Mukai 1979), it now seems clear that deleterious mutations arise at a high rate in most organisms. Summing over all loci, and to an order of magnitude, the deleterious mutation rate appears to be at least one per diploid genome per generation, and indirect evidence suggests it could be much higher (Kondrashov 1988).…”