Evolution of sex: Using experimental genomics to select among competing theories

Abstract

Few topics have intrigued biologists as much as the evolution of sex. Understanding why sex persists despite its costs requires not just rigorous theoretical study, but also empirical data on related fundamental issues, including the nature of genetic variance for fitness, patterns of genetic interactions, and the dynamics of adaptation. The increasing feasibility of examining genomes in an experimental context is now shedding new light on these problems. Using this approach, McDonald et al. recently demonstrated that sex uncouples beneficial and deleterious mutations, allowing selection to proceed more effectively with sex than without. Here we discuss the insights provided by this study, along with other recent empirical work, in the context of the major theoretical models for the evolution of sex.

General environmental heterogeneity as the explanation of sexuality? Comparative study shows that ancient asexual taxa are associated with both biotically and abiotically homogeneous environments

“…Many main concepts and their countless variants were proposed to explain the paradox of sexual reproduction (reviewed, e.g., in Bell, 1982(reviewed, e.g., in Bell, , 1985Kondrashov, 1993;Maynard Smith, 1978;Meirmans & Strand, 2010;Otto, 2009;Sharp & Otto, 2016;Williams, 1975). The genetic advantages of sex for sexually reproducing populations or individuals are highlighted by concepts such as the Weismann's idea of sex generating variability, later delimited as the hypothesis of Vicar of Bray (Bell, 1982), Fisher-Muller's accelerated evolution of sexual species (Fisher, 2003;Muller, 1932), breaking free of neighboring deleterious mutations (Crow, 1970), reduction of the spread of genomic parasites (Sterrer, 2002), advantage of diploidy (Lewis & Wolpert, 1979), repair of DNA (Bernstein & Bernstein, 2013), restoration of epigenetic signals (Gorelick & Carpinone, 2009), eventually stochastic and deterministic variants of Muller's ratchet hypothesis (Kondrashov, 1982;Muller, 1964).…”

“…Both spatial and temporal heterogeneity could be the consequences of both biotic and abiotic factors (Li & Reynolds, 1995). The temporal and spatial aspects of heterogeneity, even though differing substantially at first sight, could act remarkably similarly in terms of favoring sexual species (Kondrashov, 1993; Neiman & Schwander, 2011; Otto, 2009; Otto & Lenormand, 2002; Scheu & Drossel, 2007; Sharp & Otto, 2016; Song et al., 2011). In principle, the most important factor is always whether the environment inhabited by the offspring differs in its character (i.e., selective pressures) from the environment inhabited by their parents.…”

“…However, the predictions of different theories are not absolutely disparate—one could easily devise examples of environments suitable for asexual species according to both groups of theories, for example, stable extreme environments. Similarly, the individual theories of sexual reproduction are far from being disparate; they are usually interconnected in their basic principles, they intermingle and complement each other (Meirmans & Strand, 2010; Otto, 2009; Otto & Lenormand, 2002; Scheu & Drossel, 2007; Sharp & Otto, 2016; Song et al., 2011). Moreover, biotic and abiotic parts of the environmental heterogeneity, as well as other factors, are usually interconnected and influence and complement each other in their effects on the advantage of sexual or asexual reproduction (Glesener & Tilman, 1978; see also Otto & Lenormand, 2002; Otto, 2009; Sharp & Otto, 2016).…”

“…Similarly, the individual theories of sexual reproduction are far from being disparate; they are usually interconnected in their basic principles, they intermingle and complement each other (Meirmans & Strand, 2010; Otto, 2009; Otto & Lenormand, 2002; Scheu & Drossel, 2007; Sharp & Otto, 2016; Song et al., 2011). Moreover, biotic and abiotic parts of the environmental heterogeneity, as well as other factors, are usually interconnected and influence and complement each other in their effects on the advantage of sexual or asexual reproduction (Glesener & Tilman, 1978; see also Otto & Lenormand, 2002; Otto, 2009; Sharp & Otto, 2016). It is therefore possible that the differentiation of “biotic” and “abiotic” ecological theories of sex is important in theory, but not important in the real world, and that sexual organisms do have an advantage in environments that are both biotically and abiotically relatively heterogeneous (i.e., overall heterogeneous environments, see Table 1 and Figure 1).…”

“…Otto (2009) and Sharp and Otto (2016) identified a plethora of factors that enable the spread and long‐term predominance of sex in computer simulations, spatiotemporal heterogeneity, and varying selection pressures being among the most important. Moreover, the assumption of Flegr (2008, 2010, 2013) that the contextually dependent fitness value of alleles is a major factor in maintaining high long‐term genetic variability of sexual populations seems to be empirically supported (see Otto, 2009).…”