The Mutagenesis-Selection-Cascade Theory of Sexual Reproduction
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Article ID: WMC004367 ISSN 2046-1690 The mutagenesis-selection-cascade theory of sexual reproduction Corresponding Author: Prof. Kurt Heininger, Professor, Department of Neurology, Heinrich Heine University Duesseldorf - Germany Submitting Author: Prof. Kurt Heininger, Professor, Department of Neurology, Heinrich Heine University Duesseldorf - Germany Article ID: WMC004367 Article Type: Original Articles Submitted on:02-Sep-2013, 08:55:13 AM GMT Published on: 02-Sep-2013, 10:35:25 AM GMT Article URL: http://www.webmedcentral.com/article_view/4367 Subject Categories:REPRODUCTION Keywords:Sexual reproduction, oxidative stress, mutagenesis, Baldwin effect, epigenetics, evolvability, robustness, phenotypic plasticity, Cambrian explosion, stochasticity How to cite the article:Heininger K. The mutagenesis-selection-cascade theory of sexual reproduction. WebmedCentral REPRODUCTION 2013;4(9):WMC004367 Copyright: This is an open-access article distributed under the terms of the Creative Commons Attribution License(CC-BY), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Source(s) of Funding: None Competing Interests: None WebmedCentral > Original Articles Page 1 of 548 WMC004367 Downloaded from http://www.webmedcentral.com on 24-Sep-2013, 09:07:39 AM The mutagenesis-selection-cascade theory of sexual reproduction Author(s): Heininger K Abstract population size chances are substantial that some individuals may create beneficial mutations that provide a fitness advantage. Under environmental stress, microorganisms take advantage of their large Sexual reproduction is common in eukaryotic population sizes, create increased numbers of organisms from yeasts to humans. However, the mutations and let natural selection select the mutants question as to why sexual reproduction is so with the best fit to the actual environment. The ubiquitous is a conundrum in evolutionary biology. In evolutionary success of sexual reproduction in theory, sexual populations suffer a twofold cost multicellular organisms was dependent on solving the compared to asexual populations. A multitude of “mutator-population size dilemma”. In multicellular theories attempts to explain this conundrum, but none organisms, the large investment of scarce resources gained wider acceptance. In this comprehensive work into mature organisms limits population sizes. with more than 8,500 references I present compelling Exposing small populations of mutated organisms to evidence that it takes a joint holist and reductionist natural selection would mean a large investment into approach to solve this “queen of problems in possibly poorly viable organisms. Evolution selected evolutionary biology”. for an alternative approach: to invest as little as In a world of limited resources, the twofold cost of possible into small, mutated units and to bet-hedge sexual reproduction may only be relevant in organisms with large gamete populations. The huge energetic that live far below the carrying capacity of their habitat. investment into this “waste” production leads to Near the habitat’s carrying capacity, however, quality gonadal functional hypoxia in higher taxa and is (fitness) of offspring is much more important than associated with increased oxidative stress and genetic quantity and the theoretical twofold cost of sexual instability. During gametogenesis, oxidative stress, reproduction has no evolutionary meaning. mutagenesis and epimutagenesis increase along the Environments never remain static. They continuously phylogenetic axis, particularly in the smaller gametes, undergo changes that alter the fitness landscapes, the sperm, resulting in male-driven mutagenesis. In displacing populations towards suboptimal fitness addition to the legendary twofold cost of sex this regions. Sexual reproduction has its evolutionary roots manifold “costs of gamete overproduction” (e.g. the in a microbial stress response. Environmentally human testicular output is approx. 2,000 spermatozoa challenged microorganisms take up foreign DNA to per second), if it were non-adaptive, should definitely either use it as template for DNA repair or increase deter any organism from investing into sexual their genetic repertoire. Thus organisms that are reproduction. poorly adapted to their current environmental Gamete overproduction requires a gamete bottleneck: conditions “bet-hedge” (as part of a variety of a stochastic bottleneck inevitably would drive Muller’s stress-related responses) hoping to boost their fitness. ratchet and result in strong mutational meltdown and, What evolved as reactive process to environmental together with their low number of offspring, this would challenge was genetically accommodated in higher have detrimental effects on population fitness in higher taxa as cybernetic and proactive evolutionary engine. taxa. Only a selection-associated gamete bottleneck A multitude of both direct and circumstantial evidences ensures long-term viability of populations. Conversely, reveals the metabolic/oxidative stress, particularly of the selection-associated gamete bottleneck allows to males, under which higher taxa generate the genetic infer the (epi)mutagenic generation of gamete variation of gametes (e.g. explaining mammalian variation. Thus sexual reproduction selects the “pearls testicular extra-abdominal descent or among the pebbles” before natural selection may lower-temperature comfort zone of male fishes). possibly frustrate a larger investment into more mature Stochastic mutagenesis and epimutagenesis are organisms. Using a variety of stressors and fraught by the substantially higher risk that mutations competitive regimes as selection principle, e.g. are rather deleterious than beneficial. Therefore, the oxidative stress and competition for limited trophic evolutionary fate of mutators is inextricably linked to factors, a casacade of selective steps at the level of their effective population size: only with a large (primordial) germ cells, differentiated gametes, WebmedCentral > Original Articles Page 2 of 548 WMC004367 Downloaded from http://www.webmedcentral.com on 24-Sep-2013, 09:07:39 AM fertilization, embryos, offspring and nonrandom mating (the separation of germline and soma), and in addition select from this extreme abundance the most viable, to creating genetic variation by shuffling their genes competitive and stress resistant gametes and offspring. during sexual reproduction are able to transmit These selection principles are increasing mutational heritable somatic mutations that are acquired and and environmental robustness and selected during the organism’s lifetime. In addition, evolvability/adaptation to life in general, rather than to polyploidy, long-term seed/egg banks, and phenotypic any particular mode of life and environment. The plasticity help these organisms to face the manifold pervasive germ-soma conflict is the Red Queen that challenges of variable environments. This capacity drives the coevolutionary dynamics underlying the makes them flexible to switch habitat- and maintenance of sexual reproduction. Along the disturbance-dependently between asexual and sexual phylogenetic axis, the mutagenic spectrum and the reproduction. population size of gametes that is exposed to sexual I can show that the predictions of the genetic theories selection cascades were increased and the population of sexual reproduction (Fisher-Muller model, Muller’s size of offspring that is exposed to natural selection ratchet, Kondrashov’s hatchet) are simplistic, was reduced. As a result of this evolutionary process, incompatible with evolutionary dynamics, and based particularly male gametes represent quasi-species on fallacious post hoc, ergo propter hoc argumentation. whose quasi-species structure, however, remains In addition, it is argued that the DNA repair theory and cryptic due to their gamete bottleneck. Oxidative parasite-host conflict theory (aka Red Queen theory), stress as final common pathways of stress responses focussing on partial aspects of the resource-stress is the joint mediator of mutagenesis, epimutagenesis, ecological network are insufficient to explain the canalization and gamete quality control by gamete evolutionary success of sexual reproduction. competition. Thus both evolvability and robustness are That stochasticity is a property of evolutionary phenotypes of the same fundamental processes, mechanisms like mutation, recombination and drift has mediating “educated guess”-based innovation, been recognized earlier but I argue that stochasticity is, plasticity and phenotype conservation in the face of in addition to selection, the second pillar and environmental and genetic variation. organizing principle on which evolution is resting. Ecological resource availability and stress intensity Bet-hedging is the evolutionary risk-spreading define the distribution of sexual and asexual response to stochasticity. Sexual reproduction is the reproduction. In resource-limited, moderately stressful ultimate bet-hedging enterprise and its evolutionary habitats, the pre-selected genetic variation provided by success the selective signature of stochastic sexual mutagenesis-selection cascades determines environments. The identification of the short- and long-term benefit of sexual reproduction. stochasticity/uncertainty as input variable into the The flip side of oxidative stress-driven cybernetic machine of evolution has far-reaching mutagenesis-selection-cascades is that sexual implications