A degenerative process underlying hierarchic transitions in evolution☆
Introduction
One of the most robust global evolutionary trends is the increase in hierarchic complexity of organism bodies (Maynard Smith and Szathmáry 1995). This hierarchic trend is not merely a reflection of the adaptive diversification and increased functional efficiency that is typically assumed to be a consequence of inter-individual competition and natural selection. Hierarchic transitions in evolution exemplify a divergence from the typical logic of natural selection, though not in conflict with it. Moreover, the resulting higher-order units are understood to be subject to selection at a higher level. Hierarchic evolutionary transitions raise many of the same questions that are addressed by theories attempting to explain the evolution of “altruistic” and prosocial behaviors. Both processes involve constraint on the autonomy of lower-level entities that enables higher-order collective relations to take precedence. There have been numerous theoretical mechanisms proposed to account for the stabilization of higher-order synergistic/cooperative units such as multi-celled organisms (e.g. Buss, 1987). At present there is no widely accepted theory for explaining how collections of formerly autonomous functional individuals could spontaneously sacrifice autonomy and fall into higher-order co-dependent relationships.
In this essay I review evidence that a generic process exhibited at all levels of biological organization significantly increases the probability that unprecedented higher-order functional synergies will emerge in evolution. The process is initiated by duplication of sources of functional determination that fractionates, redistributes, and reduces the constraints imposed by purifying natural selection. Relaxation of selection decreases the costs of degraded autonomy and increases the probability that the duplicate sources will serendipitously evolve toward complementary interactions and spontaneously facilitate higher-order synergistic functional interactions. This increase in probability is because redundancy decreases the otherwise high probability that degraded functional components will be eliminated by natural selection. I survey a number of major hierarchic evolutionary transitions and show how this common mechanism is likely involved in each.
Section snippets
Hierarchic trends in evolutionary theory: a brief history
The popular image of biological evolution is often characterized as a process that tends to produce increasing complexification over time. However, the idea that there is a progressive hierarchic directionality implicit in the evolutionary process is widely criticized by biologists and evolutionary theorists. It is undeniable that over the vast span of geological time there has been an increase in the hierarchic complexity of organism forms on the earth. Indeed, complex multi-celled organisms
Major transitions and the problem of cooperation
Maynard Smith and Szathmáry (1995) argued that endosymbiotic transitions were variants of a more general pattern of major evolutionary transitions. They proposed eight major transitions, including such transitions as led to the evolution of eukaryotic cells, multicellularity, insect eusociality, and human language. They further argued that these transitions each reflect a common Darwinian challenge: explaining the origin of altruistic and cooperative relationships in the context of the ubiquity
Duplication–degeneration–complementation
A hint of an alternative approach emerged some decades ago, but it was not recognized as relevant to the conundrum about the evolution of cooperative complexity. In his book Evolution by Gene Duplication Susumo Ohno (1970) saw gene duplication as a mechanism for the creation of “new” genes that could eventually take on novel functions. This was motivated by the discovery of whole genome duplication in a number of species (e.g. in plants like domestic wheat and animals like vertebrates). In the
Gene duplication
Gene duplication is a common feature of genome evolution (Ohno, 1970; Ohta, 1994). It is probably the major source of new genes in the course of evolution. It is also a major means by which cooperative protein complexes arise in evolution (Orgel, 1977; Zhang, 2003). Thus, multiple occurrences of gene duplication over the course of evolution have produced large “families” of structurally and functionally related genes. Indeed, most genes can be recognized as members of larger families of genes
The hemoglobin family
To illustrate this, I describe two well-known examples. The first is the globin gene family, and specifically the hemoglobins. The hemoglobin protein complex contained in red blood cells in adult mammals comprises two varieties of the hemoglobin protein—alpha and beta hemoglobin—each coded by a distinct gene. The structure of the protein makes it possible to bind a special molecular formation (a porphyrin ring) within which an iron atom is suspended. It is this iron atom that provides the
Duplication and variation of regulatory genes
Perhaps the most dramatic example of the duplication, relaxation of selection, random walk degradation, and functional complementation effect is demonstrated by duplication of genes that code for proteins that bind to DNA and regulate the expression of yet other genes. This general class of genes is often referred to as regulatory genes. One consequence of this hierarchic recursive genetic relationship is that the expression of one gene can influence the expression of many other genes in
Extrinsic duplication of function: the ascorbic acid example
This interplay between aspects of Baldwinian and Waddingtonian mechanisms suggest an even more general application of this principle. For example, redundancy and masking effects can be generated extrinsically, and maintained irrespective of specific genetic inheritance. In this case, however, reduced selection on the intrinsic function that is thereby provided with redundant support from outside will allow the intrinsic capacity to degrade. With no internal functional redundancy selection can
Major hierarchic transition I: endosymbiosis
Probably the best-studied major hierarchic transitions in evolution involve the evolution of eukaryotic cells and the evolution of multicellularity. Though there are still many details to be discerned, advances in molecular and cell biology make it possible to approximately trace stages of duplication, relaxed selection, degeneration, and functional complementation leading to the hierarchic transitions in each case. In what follows, I will argue that this generic sequence of phases in the
Major hierarchic transition II: multicellularity
In an insightful monograph, somewhat cryptically titled The Evolution of Individuality, Leo Bus provided a general theory to account for the evolution of the three major kingdoms of multicellular organisms: fungi, plants, and animals. He identified a common problem of multicellularity that required a solution: how each kingdom defends against the problem of the re-emergence of lower-level cellular autonomy.
In many respects he identified a biological analogue to what the social philosopher John
Eusociality from the Duplication-Degeneration-Complementation perspective
For Darwin one of the most troubling apparent counterexamples to his theory of natural selection was the eusocial reproductive organization of ant and bee colonies. He intuited that their atypical reproductive specialization involved familial support and demonstrated the importance of reproduction over individual survival in evolution. But it was unclear to him how the distinctive traits of workers could be passed on to future generations if they never reproduced. The altruists’ failure to
Language
The last and highest-order evolutionary transition described by Maynard Smith and Szathmáry is the evolution of language. They consider it to be almost as significant a transition as the initial emergence of the genetic code. Language provides a critical tool for negotiating social cooperation and regulating prosocial behavior, as well as sharing and transmitting adaptive information from individual to individual and down the generations.
So, it follows that this approach to the evolution of
Conclusions and implications
The thrust of this analysis has been to extend the Duplication-Degeneration-Complementation (DDC) perspective and its analogues to also account for hierarchic transitions between levels of biological individuation. I have called the class of processes that include DDC and CNE, as well as those described above, inverse Darwinism. While they retain Darwin’s focus on the effects of reproduction (duplication-multiplication) and variation (degeneration), they invert the Malthusian implications that
Declaration of competing interest
I assert that there is no conflict of interest.
References (52)
The genetical evolution of social behaviour. I
J. Theor. Biol.
(1964)The genetical evolution of social behaviour. II
J. Theor. Biol.
(1964)- et al.
Cloning and chromosomal mapping of the human nonfunctional gene for L-gulono-gammalactone oxidase, the enzyme for L-ascorbic acid biosynthesis missing in man
J. Biol. Chem.
(1994) - et al.
Area patterning of the mammalian cortex
Gene duplication and the origin of proteins with novel functions
J. Theor. Biol.
(1977)Evolution by gene duplication: an update
Trends Ecol. Evol.
(2003)Nomogenesis, or Evolution Determined by Law. Translated from the Russian Edition by J. N. Rostovtsov, Cambridge, Mass
(1922)- et al.
Evolution as Entropy: toward a Unified Theory of Biology
(1988) The Evolution of Individuality
(1987)- et al.
Bird Song: Biological Themes and Variations
(1996)
Evolution and the biosynthesis of ascorbic acid
Science
The Synergism Hypothesis: A Theory of Progressive Evolution
Holistic Darwinism: Synergy, Cybernetics, and the Bioeconomics of Evolution
On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life
The Descent of Man, and Selection in Relation to Sex
The Temple of Nature or, the Origin of Society: A Poem, with Philosophical Notes. Printed for J. Johnson
The Symbolic Species: the Co-evolution of Language and the Brain
Relaxed selection and the role of epigenesis in the evolution of language
A role for relaxed selection in the evolution of the language capacity
Proc. Natl. Acad. Sci. USA
Beyond the symbolic species
Richard Goldschmidt: hopeful monsters and other 'heresies
Nat. Rev. Genet.
Preservation of duplicate genes by complementary, degenerative mutations
Genetics
The Material Basis of Evolution
The return of hopeful monsters
Nat. Hist.
Full House: The Spread of Excellence from Plato to Darwin
Irremediable complexity?
Science
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The reversibility of cellular determination: An evolutive pattern of epigenetic plasticity
2022, BioSystemsCitation Excerpt :These two-ways molecular processes allowed to define a certain cellular plasticity, which then received its empirical confirmation above all by clinical and experimental researches in the fields of cancer and stem cell biology, as well as of ageing and rejuvenation medicine and plant developmental biology. Globally, the related empirical evidence suggested that such new cellular plasticity processes could be laid out within a wider evolutive phylogenetic framework of degenerative or retrogressive processes underlying hierarchic transitions (Deacon, 2022). Nonetheless, much more empirical work is still needed to clarify the exact nature, function and structure of these new molecular mechanisms, which operate at the ontogenetic level, but that surely have spring out phylogenetically along the evolution of living systems.
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This work was partially supported by grants from Human Energy <humanenergy.io> and from the Boundaries of Humanity < boundariesofhumanity.stanford.edu>.