Daisyworld is Darwinian: constraints on adaptation are important for planetary self-regulation

The Daisyworld model demonstrates that self-regulation of the global environment can emerge from competition amongst types of life altering their local environment in different ways. Robertson & Robinson (1998. J. theor. Biol.195, 129-134) presented what they describe as a "Darwinian Daisyworld" in which the ability of organisms to adapt their internal physiology in response to environmental change undermines their ability to regulate their environment. They assume that there are no bounds on the environmental conditions that organisms can adapt to and that equal growth rates can potentially be achieved under any conditions. If adaptation could respond sufficiently rapidly to changes in the environment, this would eliminate any need for the environment to be regulated in the first place, because all possible states of the environment would be equally tolerable to life. However, the thermodynamics, chemistry and structure of living organisms set bounds on the range of environmental conditions that can be adapted to. As these bounds are approached, environmental conditions limit growth rate, and adaptations necessary for survival can also cost energy. Here we take account of such constraints and find that environmental regulation is recovered in the Daisyworld model. Hence, we suggest that constraints are an important part of a self-regulating planetary system.     

A fitness based analysis of Daisyworld

The Gaia hypothesis [Lovelock, J., Margulis, L., 1974. Atmospheric homeostasis: the Gaia hypothesis. Tellus 26, 1], that the earth functions as a self-regulating system, has never sat particularly comfortably with ideas in mainstream biology [Anon, 2002. In pursuit of arrogant simplicities. Nature 416, 247]. A lack of any clear role for evolution in the model has led to claims of teleology-that self-regulation emerges because it is pre-ordained to do so [Doolittle, W.F., 1981. Is nature really motherly? CoEvol. Q. 58-63; Dawkins, R., 1979. The Extended Phenotype. Oxford University Press, Oxford]. The Daisyworld parable [Watson, A.J., Lovelock, J.E., 1983. Biological homeostasis of the global environment--the parable of Daisyworld. Tellus B 35, 284], a simple mathematical illustration of Gaia, went some way to addressing these critiques but, despite recent success in incorporating natural selection [Stocker, S.,1995. Regarding mutations in Daisyworld models. J. Theor. Biol. 175, 495; Lenton, T.M., 1998. Gaia and natural selection. Nature 394, 439; Lenton, T.M., Lovelock, J.E., 2001. Daisyworld revisited: quantifying biological effects on planetary self-regulation. Tellus B 53, 288; Wood, A.J., Ackland, G.J., Lenton, T.M., 2006. Mutation of albedo and growth response leads to oscillations in a spatial Daisyworld. J. Theor. Biol. 242, 188], it remains a widely held view that the ideas are inconsistent with biological principles. We show that standard methodology from quantitative genetics can be used to predict the stationary states and dynamic behaviour of Daisyworlds. The system regulates its temperature due to the low-level evolutionary dynamics of competition between the thermally coupled daisies, no higher level principle is invoked. A reconciliation of Gaia with evolutionary theory may allow further development of evolutionary arguments for the existence of global self-regulatory systems.     

Darwinian evolution does not rule out the gaia hypothesis

This study explores so-called Darwinian Daisyworlds mathematically rigorously in detail. The original Daisyworld was introduced by Watson & Lovelock (1983) to demonstrate how two species of daisies regulate the global temperature of their planet through competition among these species against the rising solar luminosity, i.e. the Gaia hypothesis. Its variants are Darwinian Daisyworlds in which daisies can adapt themselves to the local temperature. Robertson & Robinson (1998) insist their Darwinian daisies lose the ability for temperature regulation on the basis of their spreadsheet simulations. Lenton & Lovelock (2000) point out that the constraints on adaptation recovers Darwinian daisies' ability of temperature regulation on the basis of their Euler-code simulations. The present study shows there exist the exact and closed-form solutions to these two Daisyworlds. The results contradict the former studies: Robertson and Robinson's daisies do regulate the global temperature even longer than non-adaptive daisies; Lenton and Lovelock's daisies are less adaptive than Robertson and Robinson's daisies because of the constraints on adaptation; the introduction of weak adaptability drives species into a dead end of evolution. Thus, the present results confirm that the Gaia hypothesis and Darwinian evolution can coexist.     

盖娅假说:在争议中发展

自从1972年Lovelock提出盖娅假说已经过去了40年,但围绕它的争议却从未停止过。盖娅假说在反对者的批评中与支持者的证明中不断发展。当前,最极端形式的盖娅假说基本上已被摒弃,尤其是那种明显带有目的论的说法。弱盖娅提出的"有机体可以影响他们的环境,有机体与环境的反馈耦合可以塑造两者的进化"这两个观点也已经是普遍接受的事实。除此之外,盖娅假说提出的其他3个命题却饱受争议。(1)内在平衡的盖娅:生物调节反馈有助于环境的内在平衡。反对者认为,生物反馈稳定全球环境的说法,与冰芯记录和大量的气候反馈研究结果相矛盾的。支持者认为,地球生物-环境系统的内在平衡可以产生于正负反馈的混合。盖娅假说关心的是地球几十亿年的历史,盖娅假说在较短时间尺度内可证伪,并不意味着其在较长时间尺度内也可证伪。(2)最优的盖娅:生物调节环境,使环境更加适合生物的生存。关于有机体的繁荣主要是由于他们对环境的改变,还是由于他们对环境的适应,目前尚未有结论。但盖娅的支持者认为,当生物-环境系统受到干扰或崩溃时,主导过程将显现。拥有较强环境反馈的系统,将易于快速过渡到新的状态,而由适应主导的过程将改变得较为平缓。反对者同意生物通过生物调节作用影响环境条件以使自身受益,但是生物首先要适应环境条件通过自然选择才能得以繁荣发展的。地球形成这样的环境条件,很可能纯粹是一种运气。(3)自然选择的盖娅:生物调节反馈产生于达尔文式的自然选择。反对者认为,"自然选择支持促进生命效应"的说法并非普遍有效,只有当遗传特征赋予携带者繁殖优势时,自然选择才会支持它。自然选择是机制,而非原则。支持者认为自然选择并不是盖娅系统环境调节的必要条件;基于副产品的自然选择,可以解决许多进化论学者提出的物种合作中的欺骗问题;自然选择并不总是支持促进生命的效应,但在当遗传特征使携带者相对非携带者受益时,自然选择可以使特征携带者产生进化优势。虽然争议依然存在并将持续下去,但作为假说生产者,盖娅假说已经证明了它的价值。但是在人类活动对生物圈影响不断增强的背景下,盖娅假说必须与人类活动相结合,否则必然走向衰落,并被其他理论或假说所替代。在此基础上,未来盖娅假说的研究者们需要继续努力探索可以应用于生物圈的一般性原则,并坚持系统性的思考方法。在具体的方法方面,可以利用系统度量指标;建立新的模型,尤其是建立关于生物地球化学循环过程的机理模型;搞清楚不同尺度过程的成本与收益。     

Gaia as a complex adaptive system

We define the Gaia system of life and its environment on Earth, review the status of the Gaia theory, introduce potentially relevant concepts from complexity theory, then try to apply them to Gaia. We consider whether Gaia is a complex adaptive system (CAS) in terms of its behaviour and suggest that the system is self-organizing but does not reside in a critical state. Gaia has supported abundant life for most of the last 3.8 Gyr. Large perturbations have occasionally suppressed life but the system has always recovered without losing the capacity for large-scale free energy capture and recycling of essential elements. To illustrate how complexity theory can help us understand the emergence of planetary-scale order, we present a simple cellular automata (CA) model of the imaginary planet Daisyworld. This exhibits emergent self-regulation as a consequence of feedback coupling between life and its environment. Local spatial interaction, which was absent from the original model, can destabilize the system by generating bifurcation regimes. Variation and natural selection tend to remove this instability. With mutation in the model system, it exhibits self-organizing adaptive behaviour in its response to forcing. We close by suggesting how artificial life ('Alife') techniques may enable more comprehensive feasibility tests of Gaia.     

Chemical Ecology and Biomolecular Evolution

The belief in the Darwinian theory of evolution appeared to be shaken when one tried to interpret statements of molecular biology in it. As a consequence there arose a theory of non-Darwinian neutral evolution. The supporters of this theory believe that under natural conditions no factors exist which can distinguish and select organisms on their internal (molecular) structure. In the opinion of these neutralists natural selection cannot in principle control the molecular constitution of organisms. Contrary to the viewpoint of the critics of neutralism it is impossible to admit that nucleic acids, proteins and other biomolecules can evolve without the participation of natural selection. This controversy in contemporary theoretical biology can be solved by integrating the conceptions of molecular ecology with Darwinian theory. Molecular ecology acknowledges the interactions of organisms by means of chemical substances synthesized by them. Such chemical ecological factors play a leading part in the selective stages of biomolecular evolution. These diverse chemical ecological interrelations take place intensively when living beings interact with parasitic microbes.     

The Origins and Evolution of Culture

This article outlines a deductive theory that creates a new way to think about the origins and evolution of culture. It is Darwinian in the sense that it posits that novel concepts and behavior, like novel genes, appear randomly and are subject to selection on the basis of specific criteria that are established by the properties of living things. The theory permits us to hypothesize properties of the genome that generate culture and to infer the conditions under which selection would favor the origins of culture. Theoretical deductions lead to the conclusion that the organisms that create culture actively participate in the creation of descendants who exhibit increasing cultural abilities and who generate increases in productivity and more reliable flows of resources. Culture is not something that has evolved solely and relatively recently in the hominid line of evolution. Fossil evidence suggests that culture may have existed at least 50 million years ago, and may have originated more than 200 million years ago.     

The consequence of maximum thermodynamic efficiency in Daisyworld

The imaginary planet of Daisyworld is the simplest model used to illustrate the implications of the Gaia hypothesis. The dynamics of daisies and their radiative interaction with the environment are described by fundamental equations of population ecology theory and physics. The parameterization of the turbulent energy flux between areas of different biological cover is similar to the diffusive-type approximation used in simple climate models. Here I show that the small variation of the planetary diffusivity adopted in the classical version of Daisyworld limits the range of values for the solar insolation for which biota may grow in the planet.Recent studies suggest that heat transport in a turbulent medium is constrained to maximize its efficiency. This condition is almost equivalent to maximizing the rate of entropy production due to non-radiative sources. Here, I apply the maximum entropy principle (MEP) to Daisyworld. I conclude that the MEP sets the maximum range of values for the solar insolation with a non-zero amount of daisies. Outside this range, daisies cannot grow in the planet for any physically realistic climate distribution. Inside this range, I assume a distribution of daisies in agreement with the MEP. The results substantially enlarge the range of climate stability, due to the biota, in comparison to the classical version of Daisyworld. A very stable temperature is found when two different species grow in the planet.     

Punctualism, non-adaptationism, neutralism and evolution

In its further development the theory of evolution will incorporate molecular biology, synergetics and the theory of information. Using a simple model it is shown that speciation can be similar to phase transition. This is a thermodynamical statement which does not say anything concerning the sharpness and kinetic features of transition. Hence there is no contradiction between punctuated equilibrium and phyletic gradualism. The notion of punctualism can be used in the sense of phase transition. Evolution is directional because of constraints of natural selection due to the structure of organisms already existing and to the possible pathways of development. Correspondingly many characters are non-adaptative. Not only are the structures of proteins important for speciation but also the exact answers to the questions: "how much", "where" and "when"? These answers can be obtained as the results of regulation of genes, particularly of homeiotic regulation. The basis features of the structure of proteins are considered and the sense of the neutral theory is discussed in connection with degeneracy of correlation between the primary structure of a protein, its spatial structure and biological function. Informational aspects of evolution are discussed. Punctualism, non-adaptationism and neutralism form the triad of internally connected features of evolution. The Darwinian theory preserves its fundamental significance.     

Natural selection without survival of the fittest

Susan Mills and John Beatty proposed a propensity interpretation of fitness (1979) to show that Darwinian explanations are not circular, but they did not address the critics' chief complaint that the principle of the survival of the fittest is either tautological or untestable. I show that the propensity interpretation cannot rescue the principle from the critics' charges. The critics, however, incorrectly assume that there is nothing more to Darwin's theory than the survival of the fittest. While Darwinians all scoff at this assumption, they do not agree about what role, if any, this principle plays in Darwin's theory of natural selection. I argue that the principle has no place in Darwin's theory. His theory does include the idea that some organisms are fitter than others. But greater reproductive success is simply inferred from higher fitness. There is no reason to embody this inference in the form of a special principle of the survival of the fittest.I would like to thank John Beatty, Ron Giere, Philip Kitcher and John Winnie for detailed and helpful criticisms of an earlier draft of this paper.     

Formation of evolutionary approach as an explanatory principle for ecology

Although the connection of ecology with evolutionary idea and specifically with Darwinism was proclaimed for a long time it seems that Herbert Spencer's approach with its emphasize on natural equilibrium was much more often used as its real theoretical base. Elements of Darwinian approach appeared only in 1920-30s in works of those few researchers who studying the distribution and population dynamics of different species tried to understand general mechanisms providing their continuing existence. Later, in the middle of 1950s the first attempts were undertaken to consider the population life history (primarily the age specific schedule of death and reproduction) as a result of natural selection aimed to maintain the necessary level of fitness. A special attention in these studies that burgeoned in 1980-90s was paid to looking for various trade-offs between particular parameters of life history, e.g., between the survival of juveniles and fecundity of adults. The problem of life history optimization became central for the whole branch of science named "evolutionary ecology". Though traditionally this branch is connected with Darwinism, it is rooted rather in Spencer's ideas on moving equilibrium and deals more with static than dynamic. Disproportionately less attention was paid to the evolution of communities since these formations could be hardly interpreted as units of Darwinian selection. Moreover, the ecologists dealing with biosphere as a unified biogeochemical system began insist on "nondarwinian" nature of its evolution. The author considers this opinion as not sufficiently grounded. Darwin's ideas about unavoidable exponential growth, intrinsic for any population, consequent deficiency of resources, and differential survival and reproduction of individuals are still useful while studying the evolution of living organisms (phylogenetics) or the development of biosphere as a global ecosystem.     

Behavioral and neural Darwinism: Selectionist function and mechanism in adaptive behavior dynamics

An evolutionary theory of behavior dynamics and a theory of neuronal group selection share a common selectionist framework. The theory of behavior dynamics instantiates abstractly the idea that behavior is selected by its consequences. It implements Darwinian principles of selection, reproduction, and mutation to generate adaptive behavior in virtual organisms. The behavior generated by the theory has been shown to be quantitatively indistinguishable from that of live organisms. The theory of neuronal group selection suggests a mechanism whereby the abstract principles of the evolutionary theory may be implemented in the nervous systems of biological organisms. According to this theory, groups of neurons subserving behavior may be selected by synaptic modifications that occur when the consequences of behavior activate value systems in the brain. Together, these theories constitute a framework for a comprehensive account of adaptive behavior that extends from brain function to the behavior of whole organisms in quantitative detail.     

Adaptive force produced by stress-induced regulation of random variation intensity

The Darwinian theory of life evolution is capable of explaining the majority of related phenomena. At the same time, the mechanisms of optimizing traits beneficial to a population as a whole but not directly to an individual remain largely unclear. There are also significant problems with explaining the phenomenon of punctuated equilibrium. From another perspective, multiple mechanisms for the regulation of the rate of genetic mutations according to the environmental stress have been discovered, but their precise functional role is not well understood yet. Here a novel mathematical paradigm called a Kinetic-Force Principle (KFP), which can serve as a general basis for biologically plausible optimization methods, is introduced and its rigorous derivation is provided. Based on this principle, it is shown that, if the rate of random changes in a biological system is proportional, even only roughly, to the amount of environmental stress, a virtual force is created, acting in the direction of stress relief. It is demonstrated that KFP can provide important insights into solving the above problems. Evidence is presented in support of a hypothesis that the nature employs KFP for accelerating adaptation in biological systems. A detailed comparison between KFP and the principle of variation and natural selection is presented and their complementarity is revealed. It is concluded that KFP is not a competing alternative, but a powerful addition to the principle of variation and natural selection. It is also shown KFP can be used in multiple ways for adaptation of individual biological organisms.     

The fittest versus the flattest: experimental confirmation of the quasispecies effect with subviral pathogens

The "survival of the fittest" is the paradigm of Darwinian evolution in which the best-adapted replicators are favored by natural selection. However, at high mutation rates, the fittest organisms are not necessarily the fastest replicators but rather are those that show the greatest robustness against deleterious mutational effects, even at the cost of a low replication rate. This scenario, dubbed the "survival of the flattest", has so far only been shown to operate in digital organisms. We show that "survival of the flattest" can also occur in biological entities by analyzing the outcome of competition between two viroid species coinfecting the same plant. Under optimal growth conditions, a viroid species characterized by fast population growth and genetic homogeneity outcompeted a viroid species with slow population growth and a high degree of variation. In contrast, the slow-growth species was able to outcompete the fast species when the mutation rate was increased. These experimental results were supported by an in silico model of competing viroid quasispecies.     

Evolution,reproduction and definition of life

Synthetic theory of evolution is a superior integrative biological theory. Therefore, there is nothing surprising about the fact that multiple attempts of defining life are based on this theory. One of them even has a status of NASA’s working definition. According to this definition, ‘life is a self-sustained chemical system capable of undergoing Darwinian evolution’ Luisi (Orig Life Evol Bios 28:613–622, 1998); Cleland, Chyba (Orig Life Evol Bios 32:387–393, 2002). This definition is often considered as one of the more theoretically mature definitions of life. This Darwinian definition has nonetheless provoked a lot of criticism. One of the major arguments claims that this definition is wrong due to ‘mule’s problem’. Mules (and other infertile hybrids), despite being obviously living organisms, in the light of this definition are considered inanimate objects. It is strongly counterintuitive. The aim of this article was to demonstrate that this reasoning is false. In the later part of the text, I also discuss some other arguments against the Darwinian approach to defining life.     

The Critical Roles of Information and Nonequilibrium Thermodynamics in Evolution of Living Systems

Living cells are spatially bounded, low entropy systems that, although far from thermodynamic equilibrium, have persisted for billions of years. Schrödinger, Prigogine, and others explored the physical principles of living systems primarily in terms of the thermodynamics of order, energy, and entropy. This provided valuable insights, but not a comprehensive model. We propose the first principles of living systems must include: (1) Information dynamics, which permits conversion of energy to order through synthesis of specific and reproducible, structurally-ordered components; and (2) Nonequilibrium thermodynamics, which generate Darwinian forces that optimize the system. Living systems are fundamentally unstable because they exist far from thermodynamic equilibrium, but this apparently precarious state allows critical response that includes: (1) Feedback so that loss of order due to environmental perturbations generate information that initiates a corresponding response to restore baseline state. (2) Death due to a return to thermodynamic equilibrium to rapidly eliminate systems that cannot maintain order in local conditions. (3) Mitosis that rewards very successful systems, even when they attain order that is too high to be sustainable by environmental energy, by dividing so that each daughter cell has a much smaller energy requirement. Thus, nonequilibrium thermodynamics are ultimately responsible for Darwinian forces that optimize system dynamics, conferring robustness sufficient to allow continuous existence of living systems over billions of years.     

What lies beneath: natural products from marine organisms as nuclear receptor modulators

The consequences for organism fitness of mutations in a given protein are often thought to be determined to a significant extent by epistasis, that is, by the fact that the effect of a mutation may be strongly dependent on the previous mutational background. Actually, a given mutation could be deleterious or beneficial depending on the background, a situation known as 'sign epistasis'. Under pervasive sign epistasis, many mutational trajectories towards a 'fitter protein' will show a 'dip' in fitness and, it has been previously suggested, only a few trajectories will be available to Darwinian selection. In this issue of the Biochemical Journal, Zhang et al. explore how this simple picture needs to be modified when two rather general and important features are taken into account, namely that many proteins are promiscuous and that living organisms must survive and thrive in environments that change continuously. The multidimensional nature of epistasis for a protein involved in several tasks, together with the fact that different tasks may become critical for organism survival as environmental conditions change, is shown by Zhang et al. to contribute to eliminating fitness dead-ends in protein sequence space. Consequently, many alternative mutational trajectories should allow protein optimization for enhanced organism fitness under changing environmental conditions.     

Mutation of albedo and growth response produces oscillations in a spatial Daisyworld

We extended a two-dimensional cellular automaton (CA) Daisyworld to include mutation of optimal growth temperature as well as mutation of albedo. Thus, the organisms (daisies) can adapt to prevailing environmental conditions or evolve to alter their environment. We find the resulting system oscillates with a period of hundreds of daisy generations. Weaker and less regular oscillations exist in previous daisyworld models, but they become much stronger and more regular here with mutation in the growth response. Despite the existence of a particular combination of mean albedo and optimum individual growth temperature which maximises growth, we find that this global state is unstable with respect to mutations which lower absolute growth rate, but increase marginal growth rate. The resulting system oscillates with a period that is found to decrease with increasing death rate, and to increase with increasing heat diffusion and heat capacity. We speculate that the origin of this oscillation is a Hopf bifurcation, previously predicted in a zero-dimensional system.