Shuffling type of biological evolution based on horizontal gene transfer and the biosphere gene pool hypothesis
Introduction
The theory of biological evolution traditionally rests on three concepts: heredity, variability and natural selection. Heredity provides transfer of genetic information from one generation to the next. Variability in the form of random mutations provides the emergence of novelties. Natural selection chooses amongst those novelties and their precursor genomes. Natural selection discards novelties that have proved lethal or simply harmful to the existence of the clone, but also allows novelties representing improvements add to the genome resulting in a new clone.
This process is slow because of the tiny probability of useful mutations. Note that mutations can vary from point mutations of the nucleotides to additions, deletions, or rearrangements of parts of genes to whole chromosomes, plus aneuploidy and polyploidy events. For example, if the mutation is of a single transcribed gene that yields a protein, its probability is a result of multiplication of the following small probabilities: probability of mutation itself; probability that the mutated gene synthesizes an RNA molecule that, in turn, synthesizes a stable protein molecule; probability of incorporation of the synthesized protein molecule into a cell's metabolic network; and finally – the probability of usefulness of the incorporated protein. It is obvious that the resulting product of probabilities is small and this notion corresponds well to the slow rate of biological evolution in the Archean and Proterozoic eons (Gordon and Mikhailovsky, 2019; Mikhailovsky, 2018b; Mikhailovsky and Gordon, 2017).
We can argue as follows that this process is stationary if not slowing down. Heredity, confined here to exact reproduction of a genome, then corresponds in an ideal case to zero variability. It works against variability and preserves genetic traits rather than changes them. Generally heredity improves its mechanisms over time which leads to slower evolution. Variability, on the contrary, accelerates biological evolution, but is based on mutagenic factors that do not increase significantly, except for short periods of the Earth's magnetic field flip-flops (Sagnotti et al., 2014; Witze, 2019). Finally, natural selection neither accelerates nor decelerates evolution. More accurately, stronger selection self-evidently implies faster mutation-driven evolution. But on the other hand, stronger selection can imply slower evolution if genetic variation is primarily supplied by recombination (Ueda et al., 2017). Because natural selection pressure in both cases influences evolution in opposite directions, its rate remains on average the same. Thus, we could expect that during the last 4 billion years of life on Earth, the rate of evolution fluctuated around some average value or gradually decreased.
However, real biological evolution was approximately stationary during only the first 3.5 billion years, i.e., in the Archean and Proterozoic eons, of respective durations of 1.5 and 1.96 billion years (Wikipedia, 2019b). A closer look, including the division of eons into epochs (Table 1) shows that such a slowdown manifested itself only at the beginning of the Proterozoic eon in the Paleoproterozoic era, that is, 2.5 to 1.6 billion years ago. From the middle of this eon (Mesoproterozoic era), biological evolution began to accelerate. This allows an approximation of the last six eras, i.e., the left six points in Fig. 1 based on data from Table 1, as an exponential curve y = a + ex where a = 4.5 and x = 7.0 (Fig. 2a). It agrees well with the exponential approximation of the increase in biological complexity by Alexei Sharov (2006).
At the same time, the right seven points of the curve in Fig. 1 from the very beginning of life (Eoarchean era) till the end of Proterozoic eon (Neoproterozoic era) could be interpreted as fluctuations around the average rate of the biological evolution that approximately equals to relative rate of Ri = 10. In this case, one could approximate as an exponential curve the last three points in Fig. 1 that relates to eras of the Phanerozoic eon. Such an exponential curve has the other values of its parameters: a = 3.2 and x = 2.8 (Fig. 2b). On the other hand, it is possible to approximate the dynamics of the rate of biological evolution throughout all its history, starting from 4 billion years ago, by combining the straight line (left) and the exponential curve (right). The best approximation of this kind (Fig. 3) shows that the switch from average constant (equals to 9.023) to exponential rate (with a = 6.3045 and x = 1.0) occurred during the Neoproterozoic era, the last one of the Proterozoic eon, simultaneously with the appearance of the first complex multicellular organisms (Table 1). In any case, at the beginning of the Phanerozoic eon the rate of evolution began to rise, obviously exponentially.
The Phanerozoic eon itself lasted only 541 million years. Of course, it is not complete yet, but mankind is changing the biosphere so radically and rapidly that the end of the current eon can be expected in the near future. (Some call the present era the Anthropocene (Wikipedia, 2019a). More important is that duration of the main milestones inside the Phanerozoic, i.e., Paleozoic, Mesozoic and Cenozoic eras, were 289, 187 and 65 million years, respectively (see Table 1). In other words, after the end of the Proterozoic eon, there is a clear acceleration of evolution, which cannot be explained by any of the three main concepts of evolution. This means that these three traditional concepts are not enough, and there is a need for a fourth concept to explain the increased evolutionary rate in the Phanerozoic eon. The purpose of this article is to formulate the fourth concept, which we call “shuffling evolution”, to be explained below.
It is not surprising that the sudden jump in the rate of evolution, dated by the very beginning of the Phanerozoic eon (the so-called “Cambrian explosion”) and the subsequent exponential evolution, still has no generally accepted explanation. The suggested options include an “ecological snowball” effect due to a series of knock-on ecological processes when environmental changes crossed critical thresholds (Zhang and Shu, 2014), increasing of bottom water oxygenation up to near modern oxygen levels (Chen et al., 2015; Zhang and Cui, 2016), sea level rise as a major factor (Smith and Harper, 2013), continental emergence (Lee et al., 2018), erosion enriching the ocean with nutrients (Maruyama et al., 2014; Santosh et al., 2014), global methane cycling (Kirschvink and Raub, 2003), extinction of the Ediacarian fauna (Darroch et al., 2018), predation (Bicknell and Paterson, 2018), interdependence between clones (Vannier, 2009), homeobox gene duplications (Holland, 2015), metamerism (Couso, 2009), head and appendage evolution (Chen, 2009), and several other options (Conway-Morris, 2003; Marshall, 2006; Zhang et al., 2014), from the impact of a life bearing comet seeding Earth with new cosmic-derived cellular organisms (Hoyle and Wickramasinghe, 1981a, 1981b; Steele et al., 2018) to divine intervention of intelligent design (Meyer, 2013). The most common point of view considers the Cambrian explosion as a result of a complex interaction of abiotic and biotic processes (Smith and Harper, 2013). It may have been due to the invention of “continuing differentiation” (Gordon, 1999; Gordon and Gordon, 2019), i.e., the ability to duplicate branches of an organism's differentiation tree (Alicea and Gordon, 2016; Gordon and Gordon, 2016; Gordon, 2013). The resulting explosive growth of the fractal tree of life (Gordon, 1992, 1999) would suggest that the Cambrian explosion is simply a mathematical consequence of the autocatalytic nature of the evolution of multicellular organisms with continuing differentiation (Gordon, 1999).
Section snippets
Horizontal gene transfer
Such rich diversity of possible explanations suggests that Phanerozoic evolution may be based on another fundamental concept of biological evolution, which has not yet been invoked. We suggest that the main contender for this role is horizontal gene transfer (HGT), also known as lateral gene transfer (LGT). HGT is transmission of a DNA fragment from one organism to another and its incorporation into the genome of the recipient that can belong to a different clone or even higher taxa. In
Possible consequences of a random mutation
Based on the numerous works referenced in the previous section, HGT not only exists but plays an essential role in evolution. Let us start by listing the consequences of a mutation of a gene (which we designate a “novelty”) that appears in a prokaryotic clone and generates a new clone. There can be three and only three such consequences:
- 1.
The novelty is a pseudogene that generally (Xu and Zhang, 2016) does not have protein coding ability (Sisu et al., 2014) and can exist and be horizontally
HGT as a chain reaction and the immortality of adaptive genes
At the moment of the first horizontal transfer of a new gene, there is only one donor clone containing this gene. If the transferred gene turns out to be lethal or harmful for the recipient clone, it is eliminated rapidly. But if the gene has become useful, it can successfully incorporate into the genome of the recipient clone. Initially, this happens only in one individual of the recipient, establishing a new clone. The population of this new clone will increase almost immediately on the
The biosphere gene pool (BGP) as a kind of biosphere's memory
Although the spreading of a gene sends it into genomes of all the clones that can accept it (in other words, for which it is useful), this does not mean that the transferred gene will remain in all such genomes. Some or even a majority of them can lose the gene because the process of gene loss occurs frequently (Albalat and Canestro, 2016) and represents a source of genetic variation (Huang, 2013). On the other hand, the chain reaction of gene transfer is obviously not limited to several years
Biological evolution as “shuffling of the deck of genes”
The next question that arises: is there a process that “reads” this chronicle, uses this memory, “recalls” the entries in this BGP, or does all this information, accumulated by countless generations of evolutionary winners, remain unclaimed and lie in vain, diverting resources necessary for its duplication in every new generation? The second alternative looks strange, and it is not surprising that this is not the case. The process that “reads” the chronicle really exists and this, as was
Accumulation of genes in the BGP and their shuffling in the history of the biosphere
In the very beginning of life on the Earth, i.e. in the very end of Hadean eon or beginning of the Archean, the number of mutations accumulated in the BGP and even more so in the individual genomes was rather small. Fortunately, because HGT was apparently of higher frequency at that time (Andam and Gogarten, 2011), this small BGP was immediately available for practically almost all of the clones, and this essentially increased the rate of spreading of novelties. Nonetheless, their fast
Some final remarks
Even if the probability of eukaryotic HGT is several orders of magnitude less than prokaryotic, and its characteristic time, respectively, is several orders of magnitude greater, such time is still negligible on the evolutionary scale. In addition, the BGP of the Late Proterozoic biosphere, well after the formation of the first eukaryotes, became richer, along with increased richness of the eukaryotic genomes. Both of these changes should have sharply increased the number of successful HGTs. As
Conclusions
Any novelty (useful gene mutation) can have only three consequences:
- 1.
The gene appears to be pseudogene that does not have protein-coding ability and can exist and even be horizontally transferred but is invisible to natural selection and evolution, except for its burden on metabolism.
- 2.
The protein encoded by the gene appears to be harmful, all the descendants of mutant die before the first HGT (horizontal gene transfer), and the gene is eliminated.
- 3.
The protein encoded by the gene appears to be
Declaration of competing interest
The authors declare no conflicts of interest.
Acknowledgement
Thanks to Natalie K. Gordon for some critical comments.
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