The Ratchet and the Red Queen: the maintenance of sex in parasites

The evolutionary stability of sexual reproduction requires advantages sufficient to overcome the substantial costs of cross-fertilization (Williams, 1975; Maynard Smith, 1978; Bell, 1982; Lively & Lloyd, 1990). Such advantages have been sought primarily among those known to be associated with the production of variable offspring (but see Bernstein et al., 1985). Of those considered, two advantages appear to remain as viable alternatives after three decades of empirical and theoretical research: mutation clearance and partial escape from coevolving parasites (West et al., 1999). Theories regarding mutation clearance fall into two general categories: stochastic and deterministic. Under the deterministic model, asexual populations have a lower mean fitness at mutation-selection balance than sexual populations (Kimura & Maruyama, 1966; Crow, 1970). The difference can be enough to maintain sex if there are strongly synergistic effects among deleterious mutations and the rate of mutation is greater that 1–2 per genome per generation (Kondrashov, 1982, 1988; Charlesworth, 1990; Howard, 1994). Recent studies have suggested that neither of these two conditions are generally met (Willis, 1993; De Visser et al., 1997; Elena & Lenski, 1997; Keightley & Eyre-Walker, 2000; Peters & Keightley, 2000). More recent theory has suggested that synergistic effects among mutations are not required to give a deterministic advantage to sex, because sexual populations are more efficient at clearing partially recessive deleterious mutations (Chasnov, 2000; Agrawal &