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Duality of Stochasticity and Natural Selection Shape the Ecology-Driven Pattern of Social Interactions: the Fall of Hamilton's Rule

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Duality of Stochasticity and Natural Selection Shape the Ecology-Driven Pattern of Social Interactions: the Fall of Hamilton's Rule Article ID: WMC004804 ISSN 2046-1690 Duality of stochasticity and natural selection shape the ecology-driven pattern of social interactions: the fall of Hamilton's rule Peer review status: No 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: WMC004804 Article Type: Original Articles Submitted on:30-Mar-2015, 03:39:51 AM GMT Published on: 30-Mar-2015, 08:50:45 AM GMT Article URL: http://www.webmedcentral.com/article_view/4804 Subject Categories:ECOLOGY Keywords:Sociobiology, inclusive fitness, kin selection, stochasticity, cooperation, altruism, mutualism, cheating, self-organization, multilevel selection How to cite the article:Heininger K. Duality of stochasticity and natural selection shape the ecology-driven pattern of social interactions: the fall of Hamilton's rule. WebmedCentral ECOLOGY 2015;6(3):WMC004804 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: no funding Competing Interests: no competing interests WebmedCentral > Original Articles Page 1 of 264 WMC004804 Downloaded from http://www.webmedcentral.com on 30-Mar-2015, 08:50:53 AM Duality of stochasticity and natural selection shape the ecology-driven pattern of social interactions: the fall of Hamilton's rule Author(s): Heininger K Abstract ecological variables. The frequent kin structure of communities is not the predominant reason for cooperation/altruism but the result of limited dispersal. Limited dispersal and the evolution of cooperation Both competition and cooperation are pervasive at all share environmental stochasticity as common cause levels of biological organization. Traditionally, the resulting in spurious relationships. The environmental theory of evolution, understood as “red in tooth and conditions that favor cooperativity discourage claw” is challenged by the mere existence of dispersal and promote philopatry, thus shaping the cooperation. As a plausible explanation of this preferential kinship structure of cooperative conundrum, Hamilton’s rule has dominated communities. Under more adverse ecological sociobiology for 50 years, but its genetic component conditions, kin competition can strongly antagonize the (relatedness) is increasingly questioned. On the other benefits of kin cooperation and inhibit the evolution of hand, there is no doubt that social interactions are cooperation in viscous populations. Not kinship but regulated by ecological (cost-benefit) factors. context-dependent, pleiotropic processes shape the Hamilton’s rule, like Darwin’s theory, implicitly dynamic sociobiological behavior of populations. assumes a stable environment. Stable environments The ecological conditions and genetic “fossil record” of favor selfish individuals that are selected to maximize social behavior in both prokaryotic and eukaryotic their fitness. Hamilton’s rule allegedly explains the microbes hold the key to understand the evolutionary paradox of altruism, that selfish individuals forego their present of cooperation in higher taxa. In microbes, own reproductive opportunities to help close kin to cooperative behavior is induced by adverse conditions, reproduce. Kin selection/inclusive fitness was particularly starvation, leading to social aggregations Hamilton’s explanation for this conundrum. But abiotic with the formation of complex patterns such as fruiting and biotic environments are not stable, but variable, bodies and biofilms. In colonies of metabolically often unpredictable. Particularly, biotic environments stressed clonal cells the competition for scarce with their manifold conflicts, Red Queen resources is decided by a fair lottery. Experiments with coevolutionary arms races, and density- and bacteria and social amoeba suggest that cell fate frequency-dependence of fitness have often chaotic ‘decisions’ (either survival as spores or cell death dynamics. Environmental stochasticity, resulting in whose remains fuel the metamorphosis of spores) are uncertain, unpredictable reproductive success, stochastic, and moreover that these ‘decisions’ are changes fundamentally the rules for the “gamble of controlled by genetically-encoded probabilities that are life”. A cybernetic model of evolution revealed the evolvable. Behind the “veil of ignorance”, the duality of stochasticity and natural selection at input competitors are not “aware” of their relative position in and output levels of the evolutionary Black Box, the competitive hierarchy. This hierarchy is determined resulting in multilevel selection of social behavior stochastically through a variety of cellular processes (Heininger, 2013, 2015). From microbes to mammals, with inherent noise that render the cells cooperation is selected-for in harsh, uncertain and heterogeneous and the lotteries fair. unpredictable environments. In stochastic environments, cooperation trades individual fitness The vast majority of cooperative systems are maximization for less variability and greater reliability characterized by dominance hierarchies with of evolutionary outcomes. Thus, the evolution of asymmetric conflicts between dominants and cooperation is a bet-hedging (risk spreading) strategy subordinates over limited reproductive opportunities. of risk-averse individuals. The biological default setting Eusocial societies, the Holy Grail of kin selection of individuals is neither selfish nor cooperative but theory, are despotic Orwellian societies that only serve ecologically context-dependent and dynamic. the reproductive needs of selfish Big Sisters and Competition and cooperation are threshold traits of Brothers that for this purpose enslave, police, and nonlinear complex systems on a continuum of suppress their worker castes by aggression and WebmedCentral > Original Articles Page 2 of 264 WMC004804 Downloaded from http://www.webmedcentral.com on 30-Mar-2015, 08:50:53 AM chemical agents. In this respect they resemble a the uncertainties of lotteries with insurance policies, unitary metazoan organism with its reproductive populations engage in nest/burrow building, social monopoly of the germline. Punishment allows the contracts with assured fitness returns and social evolution of cooperation (or anything else) in sizable queuing. Via the law of large numbers evolution groups; thus neither altruism nor inclusive fitness generated a form of automatic biological insurance gains are behaviorally or causally involved in these against idiosyncratic risk. despotic systems. Intriguingly, queen pheromones are From a systems biology perspective Hamilton’s rule is even able to suppress reproductive activity across simplistic, biased by observation selection, static, and species boundaries e.g. from honeybees to fruit flies. parochial (ignoring the world outside its limited scope, The existence of this oppressive system clearly argues i.e., both the huge majority of cooperative behaviors against the role of inclusive fitness in the evolution of targeted to nonkin and to other species and being eusociality. Nestmate recognition, the eusocial version blind to epistemological inputs e.g. from complexity of the immune system and histocompatibility complex, theory and neurobiology). Hamilton’s rule was (and has the function to ensure the reproductive monopoly. many mathematical models still are) shaped by an Within my alternative conceptual framework of colony egalitarian worldview in which autonomous individuals fitness a joint genetic-physiological-behavioral- “decide” to forego their reproduction and help their kin ecological hypothesis of eusociality in insects is to ensure the representation of their genes in the next presented. generation. In nature, however, the vast majority of In stochastic environments, reproductive success is cooperative systems are characterized by dominance unpredictable and highly variable. In taxa without hierarchies with asymmetric conflicts. The “decision” of parental brood care, particularly insects, survivorship subordinates to help is not self-determined but to reproductive maturity is extremely low. Even in enforced by despotic dominants and the prevailing eusocial insects with independent colony foundation, environmental conditions that limit the subordinates’ the vast majority of attempts to establish a colony will options for independent reproduction. In a world of fail. The extent to which immediate gains are preferred nonlinear biological processes and social interactions, over future rewards is known as future discounting. complex emergent behavior, and probabilistic theories, Individuals who grow up in environments where Hamilton’s linear and deterministic rule is a resources are scarce, competition is intense, and plausibility-based anachronism (one of Gould and mortality is high should discount the future with its Lewontin’s “just-so stories”) rooted in Newtonian uncertain benefits more heavily than individuals who thinking. Increasingly, “expanded” definitions of grow up in abundant, supportive, long-lived habitats. altruism and indirect fitness have been used to rescue On the other hand, an uncertain, unpredictable the concept. The sociobiological definition of altruism, environment selects for evolutionary gambling, and as one of
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