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Essays-Biology / Medicine/Download/8035 CRITICAL SCIENTIFIC REFLEXIONS ABOUT THE RED QUEEN HYPOTHESIS. 5 David L. ESPESSET ----------------------------- 10 72, chemin des Baumillons, F-13015 Marseille, France. [email protected] 15 1 ABSTRACT. In evolutionary sciences, the Red Queen Hypothesis deals with extinction rates over geological time. In this article, I propose a critical reflexion on this 20 hypothesis, because some implications or metaphorical applications of the hypothesis might be considered as misinterpretations of evolutionary facts. I review various scientific interpretations of evolution and their relationship with the Red Queen Hypothesis. Eventually, I propose to rename it, to correct past misinterpretations and avoid new ones. 25 KEYWORDS. Biological evolution – Darwinism – Red Queen Hypothesis – Co-evolution – Convergence – Evolutionary ecology – Laws of nature. 30 2 EVOLUTION AND CO-EVOLUTION. Biological evolution is the changing of living beings in their heritable traits over successive generations and geological time. Various evolutionary 35 processes give rise to diversity at every level of biological organisation, including the levels of taxa, species, individual organisms, cells, and molecules. Among other scientific theories, the “Modern Synthesis” [1, 2] explains the evolutionary process, mainly based upon a so-called “Darwinian” mechanism [3], which involves random mutations followed by natural selection. Another 40 mechanism, the genetic drift, explains how an allele can be randomly fixed in small sized populations [4]. During the course of evolution, many species develop close relationships with each other to ensure their survival: as one species evolves, it will somehow affect other species. These species are said to coevolve [5]. Such 45 'symbiotic' relationships keep species from becoming extinct. Among many instances of coevolving species, some are famous and have been extensively studied, such as the coevolution of pollinating Insects and flowering plants (Angiosperms) and the many examples of coevolution between parasites and hosts [6]. 50 3 THE RED QUEEN HYPOTHESIS. In 1973, Leigh Van Valen proposed his “Red Queen Hypothesis” [7], also 55 referred to as “Red Queen's”, “Red Queen's Race” or “The Red Queen Effect” (hereafter: RQ), a 'new evolutionary law' which proposes several statements: “All groups for which data exist go extinct at a rate that is constant for a given group”; “Extinction rates are similar within some very broad categories (…)”; 60 “(…) Extinction in any adaptive zone occurs at a stochastically constant rate”; “The probability of extinction of a taxon is (…) effectively independent of its age.” [7] The hypothesis thus mainly deals with extinction rates over geological 65 time, which can be summarized as follows: at more than one taxonomic level, the shapes of survivorship curves (a great number of which are shown in the original article) are consistent with the possibility that the relative probability of extinction of a taxon is approximately constant per unit of time, as observed in the paleontological record. A direct implication is that longer-lived taxa (e.g. 70 species) are not better adapted than younger taxa (their extinction rates are similar); therefore, the RQ (the probability of evolutionary change is independent of the age of the taxa). The hypothesis can be thought of in terms of organismal change, species change or process change. The RQ intends to explain two different processes: 75 1. Coevolution among competing species could lead to situations in which the 4 probability of extinction is relatively constant over millions of years, in relation with the fact that “The RQ proposes that events of mutualism (…) are of little importance in evolution in comparison to negative interactions” [7]. For instance, the RQ appears to be especially decisive in predator-prey 80 relationships. Indeed, predator-prey relationships are arguably some of the most significant types of relationships in regard to the survival of species. For example, if a prey species evolves and becomes faster over a period of time, the predator needs to adapt and evolve in order to keep using the prey as a reliable food source. Otherwise, the now faster prey will escape and the 85 predator will lose a food source and potentially become extinct. However, if the predator gets faster itself, or evolves in another way like being stealthier or a better hunter, then the relationship can continue and the predator will survive. 2. The advantage and persistence of sexual reproduction (as opposed to asexual reproduction) at the level of individuals [8]. For instance, individuals 90 living in an area with any particular parasite may prefer a mate that seems to be immune to the parasite: the resulting offspring itself would then more probably be immune to the parasite, making it more likely to survive, reproduce and pass down its genes. In other words, in species for which asexual reproduction is possible (as in many plants and 'invertebrates'), 95 coevolutionary interactions with parasites may select sexual reproduction in hosts as a way to reduce the risk of the offspring being infected (RQ applied to sexual reproduction). Numerous examples have been held up in support of the supposed validity of the RQ. Van Valen himself “see(s) here a major difference from the 5 100 usual theory of genetic selection” [7]. About molecular evolution, he also recalls that the “Constancy of the rates of protein evolution is often regarded as the most important evidence for (…) non-Darwinian evolution (…)” [7]. Van Valen also states that “the RQ, curiously, does not deny progress in evolution” [7], something Stephen Jay Gould would certainly have denied (see below). 105 Another significant implication of the RQ is that organisms must constantly adapt, evolve, and proliferate not only to gain reproductive advantage, but also simply to survive and avoid extinction while pitted against ever-evolving opposing organisms in an ever-changing environment. 6 110 THE MAIN METAPHORICAL APPLICATION OF THE RED QUEEN: A MISINTERPRETATION OF EVOLUTIONARY FACTS? The phrase "Red Queen Hypothesis" is derived from a statement that the Red Queen, a chaotic and despotic character maintaining a terrifying ruling 115 over Wonderland, makes to Alice in Lewis Carroll's “Through The Looking- Glass” (chapter two: The Garden Of Live Flowers [9]). In her dream about the looking-glass house, Alice leaves the house to look at the garden: Alice thinks it will be easier to see the garden if she first walks up to the top of the hill, to which a straight path seems to lead. At the top of the hill, the Red Queen 120 starts running, faster and faster. Alice runs after the Red Queen but is perplexed to find that neither of them seems to be moving. When they stop running, they are exactly in the same place. Alice remarks on this, and the Red Queen responds: "Now, here, you see, it takes all the running you can do 125 to keep in the same place". What appears to me as the main – and most questionable – application of the RQ is that evolutionary change might be necessary to stay in the same place, or, to put it differently, that ever-evolving living organisms would be seen as staying in the same place. In this view, species have to 'run' (evolve) 130 in order to 'stay in the same place' (survive to be extant). It generally seems that such subsequent uses of the RQ have tacitly assumed that the words ('run' and 'stay in the same place') are to be interpreted metaphorically, as Van Valen himself apparently did. 7 But, even metaphorically, do living organisms really 'stay in the same' 135 place as they evolve? To me, such a point of view is a fundamental misinterpretation of basic evolutionary facts. In the following sections, I will review several scientific interpretations of evolution and their relationship with the RQ. 140 “Neo-Darwinian orthodoxy”. In the neo-Darwinian view of evolution [10, 11], on the basis of random mutations followed by natural selection, evolution has no particular 'goal' except that of adapting living organisms to their fluctuating environment (this refers to the everlasting debate about finality versus finalism; see below). But 145 what appears to be 'adapted' today may well be 'non adapted' tomorrow: if the environment changes, then organisms must adapt to the new conditions, otherwise they will simply disappear. In this respect I agree: when organisms evolve, they literally 'keep in the same place'. Moreover, most evolutionary biologists state that evolving organisms do not 'progress' [12], they merely 150 'change'. There would be no progress in nature, no race towards complexity, no evolutionary trends, no evolutionary strategies and evolution would be totally aimless [11], like the entire universe itself, incidentally. Some evolutionary biologists even state that 'complexity' is a useless notion in biology [13]. This school of thought is related to 'reductionism' in science. 155 8 From the “Modern Synthesis” to the “Extended Evolutionary Synthesis”. 160 But this “Darwinian evolution”, sometimes referred to as “ultra- Darwinism”, is now more and more controversial. More precisely, without ruling out the existence of Darwinian mechanisms to explain some aspects of biological evolution (like micro-evolution), it appears that other distinct evolutionary mechanisms may well be working in nature. For instance niche 165 construction, developmental bias, plasticity, lateral gene transfers and extra- genetic inheritance [14, 15, 16]. These mechanisms are part of the “Extended Evolutionary Synthesis” [17, 18]. I doubt that this synthesis is compatible with the idea of organisms metaphorically 'keeping in the same place' at the species level. 170 Consider earthworms and their ability to modify the soil they inhabit to make it a better place for their need of humidity and wet dirt. As Laland et al. state [14], physiologically, earthworms are aquatic annelids. Through a niche construction process, they are able to restructurate the soil environment to enhance water retention and accessibility. This creates for them a new 175 adaptive interface, one that is better suited to earthworms' essentially aquatic physiology.
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