The low cost of recombination in creating novel phenotypes

Wagner, Andreas

doi:10.1002/bies.201100027

Cited by 14 publications

(13 citation statements)

References 85 publications

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“…Our finding that recombination promotes the appearance of 434 multiple stable equilibria in neutral networks has clear implications for the evolution of 435 robustness and evolvability that deserve further investigation. For example, Wagner[94] 436…”

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confidence: 99%

Emergent speciation by multiple Dobzhansky-Muller incompatibilities

Paixão

Azevedo

2014

Preprint

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The Dobzhansky-Muller model posits that incompatibilities between alleles at different loci cause speciation. However, it is known that if the alleles involved in a Dobzhansky-Muller incompatibility (DMI) between two loci are neutral, the resulting reproductive isolation cannot be maintained in the presence of either mutation or gene flow. Here we show that speciation can emerge through the collective effects of multiple neutral DMIs that cannot, individually, cause speciation-a mechanism we call emergent speciation. We investigate emergent speciation using models of haploid holey adaptive landscapes-neutral networks-with recombination. We find that certain combinations of multiple neutral DMIs can lead to speciation. Furthermore, emergent speciation is a robust mechanism that can occur in the presence of migration, and of deviations from the assumptions of the neutral network model. Strong recombination and complex interactions between the DMI loci facilitate emergent speciation. These conditions are likely to occur in nature. We conclude that the interaction between DMIs may cause speciation. Author SummaryMost species are kept distinct by incompatibilities between the genes they carry. These genetic incompatibilities cause hybrids between the species to have low fitness. Here we 1/33 propose that combinations of several incompatibilities can collectively cause the origin of species, although they cannot do so acting alone-a mechanism we call emergent speciation. We use flat fitness landscapes with many holes in them to extend the classic Dobzhansky-Muller model, and capture the essence of the phenomenon. We find that emergent speciation can, indeed, occur through the combined effects of multiple genetic incompatibilities. Furthermore, the conditions that facilitate emergent speciation are likely to occur in nature. We conclude that the interaction between genetic incompatibilities may be a root cause of the origin of species. Introduction 1 Unravelling the ways in which reproductive barriers between populations arise and are 2 maintained remains a central challenge of evolutionary biology. The Dobzhansky-Muller 3 model posits that speciation is driven by intrinsic postzygotic reproductive isolation 4 caused by incompatibilities between alleles at different loci [1-3]. The kinds of strong 5 negative epistatic interactions envisioned by this model are common between amino acid 6 substitutions within proteins [4, 5]. Furthermore, Dobzhansky-Muller incompatibilities 7 (hereafter DMIs) have been shown to cause inviability or sterility in hybrids between 8 closely related species, although the extent to which any particular DMI has actually 9 caused speciation remains an open question [6-9]. 10 In Fig. 1A, we illustrate a simple version of the evolutionary scenario originally 11 proposed by Dobzhansky [1] with an incompatibility between neutral alleles at two loci 12 (A and B) in a haploid-that is, a neutral DMI [10]. An ancestral population is fixed for 13 the ab genotype. This population splits into two geographic...

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confidence: 99%

Emergent speciation by multiple Dobzhansky-Muller incompatibilities

Paixão

Azevedo

2014

Preprint

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“…This mechanism is crucial for evolutionary innovations, because genotypes which control gene-gene interactions can change profoundly without affecting phenotypes which represent gene activities or expression concentrations [2]. Wagner's GRN model motivates research on the evolution of genetic networks, and has been successfully employed to study many fundamental evolutionary and ecological questions [15,16,17,18,19,20,21,22,23,11,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52] (See [12] for an in-depth review).…”

Section: Introductionmentioning

confidence: 99%

Convergence Analysis and Network Properties of Wagner's Artificial Gene Regulatory Network Model

Wang

2019

JAMCS

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The gene regulatory network (GRN) is essential to life, as it governs all levels of gene products that enable cell survival and numerous cellular functions. Wagner's GRN model, which has mathematical roots origin from the Ising model and neural networks, is a powerful computation tool that helps integrate network thinking into biology, and motivated a new research theme focusing on the evolution of genetic networks. However, except the formal mathematicalfoundation described in [1], few papers have focused on providing further mathematical analysis of the model. Moreover, network characteristics of Wagner's GRN model when varying key parameters are unclear. Therefore, in this paper, I present a convergence analysis of Wagner's GRN model by using the Markov chain theory. I show mathematically that if we consider the evolution process as an optimisation process, then the probability of nding the optimal conguration (a certain target phenotype) converges to probability one. In addition, I investigate network characteristics such as stability, robustness and path length in initial populations. I find that generally small networks with a sparse connectivity have a higher initial stability.The robustness is also observed to be higher in initial stable networks with a low network connectivity. These results are partly explained by the pattern, as shown in this paper, that small networks with a sparse connectivity generally have a shorter path length and, therefore, they are not only able to quickly reach equilibrium phenotypic states but also more likely to resist genetic perturbations.

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“…For decades, researchers have been making tremendous efforts and proposing numerous theories to uncover the mys-tery of sex and recombination (Eshel and Feldman, 1970;Hurst and Peck, 1996;West et al, 1999;Otto and Lenormand, 2002;Meirmans and Strand, 2010;Wagner, 2011). Two classic benefits of sexual reproduction are nevertheless still controversial: 1) purging deleterious mutations more efficiently, and 2) creating novel gene combinations (Kondrashov, 1993;Otto and Feldman, 1997;Otto and Gerstein, 2006;Kouyos et al, 2007;Barton, 2009;Martin and Wagner, 2009).…”

Section: Introductionmentioning

confidence: 99%

“…An important third possibility is that the process of recombination, by allowing the localisation of both coherence and variation across the genomes of a population, is able to both improve robustness and facilitate evolutionary adaptation, a process known as evolvability (Wang et al, 2014). Although robustness and facilitated adaptation are observed phenomena, and are often attributed to sexual reproduction, the underlying mechanisms are still poorly understood (Wagner, 2011).…”

Section: Introductionmentioning

confidence: 99%

Recombination Is Surprisingly Constructive for Artificial Gene Regulatory Networks in the Context of Selection for Developmental Stability

Wang

Lan

Weinreich

et al. 2015

07/20/2015-07/24/2015

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Recombination is ubiquitous in multicellular plants, animals and even fungi. Many studies have shown that recombination can generate a great amount of genetic innovations, but it is also believed to damage well-adapted lineages, causing debates over how organisms cope with such disruptions. Using an established model of artificial gene regulatory networks, here we show that recombination may not be as destructive as expected. Provided only that there is selection for developmental stability, recombination can establish and maintain lineages with reliably better phenotypes compared to asexual reproduction. Contrary to expectation, this does not appear to be a simple side effect of higher levels of variation. A simple model of the underlying dynamics demonstrates a surprisingly high robustness in these lineages against the disruption caused by recombination. Contrary to expectation, lineages subject to recombination are less likely to produce offspring suffering truncation selection for instability than asexual lineages subject to simple mutation. These findings indicate the fundamental differences between recombination and high mutation rates, which has important implications for understanding both biological innovation and hierarchically structured models of machine learning.

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The low cost of recombination in creating novel phenotypes

Cited by 14 publications

References 85 publications

Emergent speciation by multiple Dobzhansky-Muller incompatibilities

Emergent speciation by multiple Dobzhansky-Muller incompatibilities

Convergence Analysis and Network Properties of Wagner's Artificial Gene Regulatory Network Model

Recombination Is Surprisingly Constructive for Artificial Gene Regulatory Networks in the Context of Selection for Developmental Stability

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