Sexual reproduction reshapes the genetic architecture of digital organisms

Ecology, Evolutionary Biology and Behavior Program, Michigan State University, East Lansing, MI 48824, USA.
Proceedings of the Royal Society B: Biological Sciences (Impact Factor: 5.05). 03/2006; 273(1585):457-64. DOI: 10.1098/rspb.2005.3338
Source: PubMed


Modularity and epistasis, as well as other aspects of genetic architecture, have emerged as central themes in evolutionary biology. Theory suggests that modularity promotes evolvability, and that aggravating (synergistic) epistasis among deleterious mutations facilitates the evolution of sex. Here, by contrast, we investigate the evolution of different genetic architectures using digital organisms, which are computer programs that self-replicate, mutate, compete and evolve. Specifically, we investigate how genetic architecture is shaped by reproductive mode. We allowed 200 populations of digital organisms to evolve for over 10 000 generations while reproducing either asexually or sexually. For 10 randomly chosen organisms from each population, we constructed and analysed all possible single mutants as well as one million mutants at each mutational distance from 2 to 10. The genomes of sexual organisms were more modular than asexual ones; sites encoding different functional traits had less overlap and sites encoding a particular trait were more tightly clustered. Net directional epistasis was alleviating (antagonistic) in both groups, although the overall strength of this epistasis was weaker in sexual than in asexual organisms. Our results show that sexual reproduction profoundly influences the evolution of the genetic architecture.

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Available from: Charles Ofria, Jan 07, 2014
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    • "Thus, evolution in Avida is open-ended, sometimes leading to surprising conclusions (Wilke et al. 2001) that might be missed in models lacking key elements such as mutational bias. Although Avida has previously been used to study evolution in microbe-like systems (Lenski et al. 1999; Wilke et al. 2001; Lenski et al. 2003; Chow et al. 2004; Misevic et al. 2006; Clune et al. 2011), we added new features resembling those found in more complex organisms, specifically the ingredients necessary for mate choice to evolve: sexual recombination (Misevic et al. 2006) with distinct mating types (males and females), and configurable sex-specific reproductive costs reflecting the differential investments (anisogamy) made by each sex in most animals; CPU instructions allowing organisms to develop display traits; and CPU instructions allowing females to exhibit directional mating preferences, analogous to sensory biases thought to trigger the evolution of new mate preferences (Fuller et al. 2005; Fuller 2009; Egger et al. 2011), with configurable costs for these mating preferences. Mating occurs in an area similar to a lek, with a number of competing males displaying at any given time, and females choosing among them. "
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    ABSTRACT: Mate choice and sexual displays are widespread in nature, but their evolutionary benefits remain controversial. Theory predicts these traits can be favored by runaway sexual selection, in which preference and display reinforce one another due to genetic correlation; or by good genes benefits, in which mate choice is advantageous because extreme displays indicate a well-adapted genotype. However, these hypotheses are not mutually exclusive, and the adaptive benefits underlying mate choice can themselves evolve. In particular, examining how and why sexual displays become indicators of good genes is challenging in natural systems. Here, we use experimental evolution in "digital organisms" to demonstrate the origins of condition-dependent indicator displays following their spread due to a runaway process. Surprisingly, handicap-like costs are not necessary for displays to become indicators of male viability. Instead, a pleiotropic genetic architecture underlies both displays and viability. Runaway sexual selection and good genes benefits should thus be viewed as interacting mechanisms that reinforce one another.
    Full-text · Article · Jan 2013 · Evolution
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    • "As Dennett (2002, p. E83) has emphasized, " evolution will occur whenever and wherever three conditions are met: replication, variation (mutation), and differential fitness (competition). " The Avida system fulfills all of these conditions, and it is thus a tractable model for investigating the general properties of evolving systems (Lenski et al. 1999, 2003; Adami et al. 2000; Wilke et al. 2001; Chow et al. 2004; Goings et al. 2004; Misevic et al. 2006; Pennock 2007; Clune et al. 2008, 2010). "
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    ABSTRACT: Biologists have long debated whether ontogeny recapitulates phylogeny and, if so, why. Two plausible explanations are that (i) changes to early developmental stages are selected against because they tend to disrupt later development and (ii) simpler structures often precede more complex ones in both ontogeny and phylogeny if the former serve as building blocks for the latter. It is difficult to test these hypotheses experimentally in natural systems, so we used a computational system that exhibits evolutionary dynamics. We observed that ontogeny does indeed recapitulate phylogeny; traits that arose earlier in a lineage's history also tended to be expressed earlier in the development of individuals. The relative complexity of traits contributed substantially to this correlation, but a significant tendency toward recapitulation remained even after accounting for trait complexity. This additional effect provides evidence that selection against developmental disruption also contributed to the conservation of early stages in development.
    Full-text · Article · Sep 2012 · The American Naturalist
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    • "I conducted my experiments using Avida (Ofria and Wilke, 2004), an artificial life program designed to study questions in evolution, e.g., the complexity of epistasis (Lenski et al., 1999), the effect of mutational robustness on evolvability (Elena and Sanjuán, 2008), and the genetic architecture of sexual organisms (Misevic et al., 2006). Digital organisms in Avida consist of a sequence of computer instructions that encodes their ability to replicate and perform Boolean logic operations (or 'tasks'). "
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    ABSTRACT: Evolutionary adaptation to a new environment depends on the availability of beneficial alleles. Beneficial alleles may appear as new mutations or may come from standing genetic variation—alleles already present in the population prior to the environmental change. Adaptation from standing genetic variation in sexually-reproducing populations is expected to be faster than from new mutations because beneficial alleles from standing genetic variation occur at a higher starting frequency and are immediately available. The distribution of fitness effects of alleles from standing genetic variation are expected to be different from that of new mutations because standing genetic variation has been ‘pre-tested’ by selection. Whether adaptation uses standing genetic variation or new mutations as a source of beneficial alleles is unknown. In this study, I conducted experimental evolution of digital organisms to determine the source of beneficial alleles during adaptation. I also tested the speed of adaptation and the fitness effect of alleles under these two sources of genetic variation. I found that the major source of beneficial alleles after an environmental change was standing genetic variation, but new mutations were necessary for long-term evolution. I also found that adaptation from standing genetic variation was faster than from new mutations, and the mean fitness effect of alleles from standing genetic variation were neutral, whereas new mutations were deleterious. Interestingly, I found that an important advantage of standing genetic variation was that recombination appeared to bring together beneficial combinations of alleles from standing genetic variation. These results support the hypothesis that adaptation occurs mostly from standing genetic variation and provide an additional advantage for such adaptation.
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