The Evolution of Condition-Dependent Sex in the Face of High Costs

By Hadany, Lilach; Otto, Sarah P. | Genetics, July 2007 | Go to article overview

The Evolution of Condition-Dependent Sex in the Face of High Costs


Hadany, Lilach, Otto, Sarah P., Genetics


ABSTRACT

Facultatively sexual organisms often engage in sex more often when in poor condition. We show that such condition-dependent sex carries evolutionary advantages and can explain the evolution of sexual reproduction even when sex entails high costs. Specifically, we show that alleles promoting individuals of low fitness to have sex more often than individuals of high fitness spread through a population. Such alleles are more likely to segregate out of bad genetic backgrounds and onto good genetic backgrounds, where they tend to remain. This "abandon-ship" mechanism provides a plausible model for the evolution and maintenance of facultative sex.

(ProQuest-CSA LLC: ... denotes formulae omitted.)

THE evolution of sex has long been a puzzle to evolutionary biologists (Michod and Levin 1988; Feldman et al. 1996; Barton and Charlesworth 1998; OttoandLenormand2002). Sexual reproductiontends to break up favorable genetic associations generated by selection (Altenberg and Feldman 1987). Even if sex were entirely cost free, evolution would not always favor increased rates of recombination, requiring synergistic epistasis (Feldmanetal. 1980;Kondrashov1988;Barton 1995), frequent environmental changes (Charlesworth 1976; Barton 1995), or random genetic drift in the presence of recurrent selection (Felsenstein 1974;Otto and Barton 1997; Otto and Barton 2001; Keightley and Otto 2006). To complicate matters, sexual reproduction is often very costly: producing males can, in the absence of paternal care, double the cost of reproduction. In addition, sexual organismshave tofindandcourt a partner and then mate, thus wasting time and energy and exposing themselves to predation, disease transmission, and potential conflicts between the sexes. Despite all of the above, sexual reproduction is common among eukaryotes.

The majority of studies on the evolution of sex focus either on the evolution of recombination rates (see reviews by Feldman et al. 1996; Barton and Charlesworth 1998; Otto and Lenormand 2002) or on the long-term consequences of sex to the mean fitness and competitive ability of a population (e.g., Muller 1964; Kimura andMaruyama 1966; Kondrashov 1988;Howard and Lively 1994; Peck et al. 1997; Chasnov 2000; Agrawal and Chasnov 2001; Hadany and Feldman 2005). Fully understanding the evolution and maintenance of sex, however, requires that we consider populations capable of both sexual and asexual reproduction and investigate when increased investment in sexual reproduction can evolve. Facultative sex is common among plants, fungi, protists, and other organisms (Bell 1982) and is likely to be the mode of reproduction among the first sexual eukaryotes (Dacks and Roger 1999).

In this article, we consider how investment in sexual function evolves within facultatively sexual species if the tendency to reproduce sexually is condition dependent. Recent studies have found that alleles increasing the likelihoodof reproducing sexually (independent of condition) can increase in frequency due to the advantages of segregation, as long as some inbreeding occurs within a population and dominance levels lie within specified regions (Dolgin and Otto 2003; Otto 2003).

These studies have assumed, however, that facultatively sexual species undergo sex at a constant rate. In reality, the frequency of sex generally depends on the condition of an individual, a pattern found broadly across both facultatively sexual prokaryotes and eukaryotes (Bell 1982). Individuals that are starved undergo sex at higher rates in a wide variety of organisms, including bacteria (Dubnau 1991; Redfield 1993; Jarmer et al. 2002; Foster 2005), yeast (Kassir et al. 1988; Mai and Breeden 2000), Chlamydomonas reinhardtii (Harris 1989), and daphnia (in combination with photoperiod and density cues; Kleiven et al. 1992). Cells with DNA damage have also been shown to undergo sex at higher rates inviruses (Bernstein 1987), bacteria (Wojciechowski et al. …

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