Riddle of Sex. Cui prodest: gene, individual, group? Column for Kompyuterra #131

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Dmytro Shabanov
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Column for Kompyuterra #130 Column for Kompyuterra #131 Column for Kompyuterra #132 Well, there: I've outlined the program for my future columns myself, and now I have to fulfill it! It's a holiday time, decent people's heads are occupied—some with preparing for the festive table, some with decorating the New Year tree, some with composing New Year wishes. And I will have to fulfill my own promise and discuss the problem of sexual reproduction. Well, let's consider that the topic of sex itself is festive enough. Alas, I won't be able to close it in one column. Let me do this: I'll offer you a New Year column with many pictures illustrating the origin of sexual reproduction. This column will end with a question, my version of the answer to which I will give only next year. I will be glad to hear (see in the comments) yours. I'll start from afar. You probably know that earthly organisms have two fundamentally different cell types—prokaryotic (pre-nuclear) and eukaryotic (nuclear). It is considered that of the three superkingdoms (the highest systematic categories), two, Bacteria and Archaebacteria, belong to prokaryotes. Their genetic diversity, at least approximately, can be estimated using the following scheme. [IMG_1] This is the most general dendrogram (scheme showing the branching pattern of the "tree of life") describing the relations between the main groups of earthly organisms. Here you can examine its basis in more detail. Do you think that animals occupy disproportionately little space on this scheme? Yes, the disproportion is evident, but it is of the opposite character. The scheme reflects genetic diversity, and it actually gives disproportionately much attention to the kingdoms Plants, Fungi, and Animals—small twigs on the branch of the kingdom Protists (where "protists" like amoebas and ciliates, various algae, and many unicellular fungus-like organisms belong). And all these four kingdoms of eukaryotes represent only a small part of the genetic diversity of prokaryotes. On the other hand, if we were to reflect the number of species, the representatives of the multimillion-strong kingdom Animals would overwhelm the other groups. [IMG_2] An enlarged fragment of the same scheme. When presenting schemes, we need to understand how they are constructed. Phylogenetic (reflecting evolutionary history) relations are reconstructed from genetic data using algorithms that build branching trees so as to minimize the assumed number of evolutionary changes (I wrote about parsimonious phylogeny reconstruction in the column about the pegasofer beast). When it comes to reconstructing relations within the kingdom Animals, this approach turns out to be relatively adequate. However, the origin of plants or the emergence of the very superkingdom Eukaryotes is reconstructed with inevitable distortions. The thing is that the eukaryotic cell arose as a result of symbiosis of several prokaryotic cells. I won't go into details now and will limit myself to a fairly simple (and therefore relatively conditional) scheme. Among other things, this scheme does not reflect that in some groups we register the consequences of repeated symbioses. [IMG_3] Symbiogenetic origin of the eukaryotic cell (simplified, very simplified scheme!) Thus, the cytoplasm (main content) and nucleus of animal cells arose from an ancestral archaebacterium, and mitochondria—from an ancestral alphaproteobacteria (a representative of the same group of eubacteria to which, for example, the wolbachia mentioned in the previous column belongs—an intracellular parasite/symbiont of arthropods, capable of causing parasite-induced parthenogenesis). Some of the genes belonging to the mitochondrial ancestor moved from the mitochondria to the nucleus. Does it surprise you that this could happen? Very simple. A mitochondria (like any other intracellular symbiont) can die and disintegrate. Its DNA will be released into the cytoplasm of the host cell and, after some journeys, can integrate into the host DNA. There is a possibility that the nucleus will start producing those proteins that the mitochondria used to assemble for itself. Receiving these proteins from the host cell, the mitochondria will increase the efficiency of its work, and such a change can be supported by selection. However, now selection will no longer support the functionality of the original gene in the mitochondria itself. Over time, this gene will degenerate and disappear in the mitochondria, and a functional copy will remain in the nucleus. How do our reconstruct the prehistory of such a chimeric cell? Examining originally nuclear genes, they will bring such a hybrid cell closer to the relatives of its cytoplasm and nucleus (in our example—to archaebacteria, as shown in the scheme). Examining genes of mitochondrial origin, these algorithms will find its closest relatives among alphaproteobacteria. The reticulate nature of phylogeny cannot be reflected in the structure of a branching tree, and typical phylogeny reconstruction algorithms can only construct such trees! Phylogeny reconstruction of prokaryotes is even more complex, since their genes "wander" from group to group as a result of horizontal transfer (transmission between unrelated organisms; "vertical" transmission is considered to be from ancestors to descendants). Our tools for phylogeny reconstruction turn out to be inadequate for reconstructing such relations. We need to develop new ones—and only then construct something like the schemes shown below. [IMG_4] On the left—a semi-conditional "reticulate" scheme showing relations between the three superkingdoms (source). At the basis of the scheme is a network that resulted from numerous horizontal transfers. On the right—a "ring" scheme of evolution of the main groups of bacteria (source). The most diverse group, Gram-negative (to which, among others, the ancestors of mitochondria and chloroplasts belong), is considered here as a result of symbiosis of two other groups, actinobacteria and clostridia. And what about LUCA, the "last universal common ancestor," shown on the first scheme? I agree with those who consider that LUCA was not a separate species but a complex community, whose members exchanged genes as they saw fit. You know, why was I telling you about prokaryote phylogeny reconstruction? To convince you: prokaryotes have succeeded in recombination, in forming new combinations of genetic information. Various types of recombination are distinguished (if you want to understand in detail—I highly recommend these and these articles). Of them, for our further conversation, homologous recombination is the most interesting. Imagine an E. coli cell, the best-studied bacterium, that has received a fragment of foreign DNA. In the cytoplasm of these bacteria there can be a plasmid, a small circular DNA molecule called the F-factor. A bacterium possessing the F-factor can grow a pilus (something like a pipeline) and pump through it, first, a copy of the F-factor, and second, copied fragments of the bacterial chromosome. [IMG_5] Do you know what these three E. coli bacteria are doing? They are exchanging fragments of their DNA through pili, constructions resembling syringe needles (source). The donor cell can use foreign DNA fragments for homologous recombination. In this case, it establishes correspondence between the received DNA fragment and its own cell DNA. A special protein system of the donor cell replaces the existing genetic text with the received one. An important feature of homologous recombination is that the new genetic text is inserted not just anywhere, but precisely at that place on the bacterial chromosome where its "native" version was located. New genes get into those regions where the systems controlling their activity are located. In homologous recombination in bacteria, we can see one of the stages in the formation of that form of homologous recombination which is characteristic of eukaryotes. I am talking about sexual reproduction. Strictly speaking, sexual process is not necessarily connected with reproduction. Both in E. coli and, for example, in ciliates (eukaryotic organisms), the sexual process proceeds on its own, and reproduction—seems to be on its own as well. But still the most characteristic for eukaryotes turns out to be the haplo-diploid life cycle with fertilization and meiosis. It needs explanation. I have done this once before, but I will repeat it now, otherwise (you can compare the two explanations for better understanding). Let's start with this. Depending on the number of sets of genetic information (chromosome sets) contained in the nucleus, eukaryotic cells are divided into haploid (one set), diploid (two chromosome sets), and a whole range of other types, which are not important for us now. There are two main types of eukaryotic cell division. In mitosis, the amount of genetic information does not change; two cells are formed, genetically identical both to each other and to the mother cell. In meiosis (which, in essence, consists of two divisions resembling mitosis, but not providing for the doubling of genetic information between them), four cells are obtained with halved amount of genetic information. All these cells are genetically unique, because homologous recombination occurs between homologous pairs of chromosomes. [IMG_6] Comparison of the two main types of eukaryotic cell division. If meiosis halves the number of chromosomes, then in a life cycle where it occurs, something must happen that compensates for their normal amount. This is fertilization, the fusion of two cells, consisting of two stages—syngamy (fusion of cytoplasm) and karyogamy (fusion of nuclei). [IMG_7] Example of a haplo-diploid life cycle with fertilization and meiosis. Could such a complex invention have arisen independently many times in the course of life's evolution, in different groups? In the scheme I drew, mitoses are shown only on the diploid phase, as is usually the case in highly organized animals, including humans. This is not the only solution. There are species in which mitoses and organism growth occur on the haploid phase, and the diploid phase turns out to be very short (immediately after fertilization, the zygote divides by meiosis). In most plants, growth occurs on both phases. In mosses, the haploid phase predominates, and in flowering plants, for example—the diploid phase. Now it's clear? And, of course, the most interesting is how such a complex life cycle could arise in highly organized eukaryotes. Its different stages arose separately, and to this day they are observed separately in some protists and fungi. Some eukaryotes have their own (quite complex) mechanisms providing syngamy (for example, the fusion of individual fungal filaments). Many multinucleate eukaryotes are known; in some of them karyogamy has been noted. As I already said, meiosis includes a highly organized mechanism of homologous recombination, simpler forms of which arose even in prokaryotes. There are good grounds to suppose that meiosis evolved as a form of restoration, repair (reparation) of the cell's genetic apparatus—and only later became an indispensable stage of the haplo-diploid life cycle. A number of authorities suppose that the haplo-diploid life cycle with fertilization and meiosis arose in the course of evolution not once! This is evidenced by the fact that the intimate molecular mechanisms providing these essential cell reorganizations turn out to be different in different groups. An additional circumstance supporting this assumption is the distribution of syngamy, karyogamy, and meiosis among various groups of protists: in many of their types, these phenomena are registered in advanced representatives and absent in primitive ones. If this is so, we become convinced that the transition to such a life cycle is a regular event in the evolution of many groups of eukaryotes. And now the time has come to ask the question for which I wrote this column. It concerns the level of selection responsible for the appearance of sexual reproduction. I have had to write that the problem of the level at which selection occurs is the subject of fierce dispute among many biologists: —Charles Darwin supposed that evolution is the result of selection of individuals, and sometimes—of their groups; —Vero Wynne-Edwards considered group selection to be the leading mechanism of evolution; —George Williams shattered many of Wynne-Edwards' arguments, substantiating that evolution is driven practically exclusively by individual selection; —Richard Dawkins, developing the ideas of William Hamilton and many other theorists (including Edward Wilson), declared that evolution is driven by the selection of individual genes; —Edward Wilson changed his point of view and declared the importance of group selection for some key evolutionary transitions; —many biologists of the older generation fundamentally deny the idea of the "selfish gene" —many young biologists (especially molecular biologists, not accustomed to thinking about general questions) are convinced that "modern" biology has "proven": selection proceeds only at the level of genes. Thus, biology is shaken by discussions about the "selfish gene," "selfish individual," and "selfish group." So, attention: the question! Selection of which level (gene, individual, or group) is the cause of the transition to sexual reproduction? And, if you want, a hint. In those cases when some evolutionary innovations promote the preservation and reproduction of both genes and individuals and groups, we will not be able to establish which level of selection is responsible for their development. We need to look for such changes that, let's say, are advantageous for the reproduction of the genes causing these changes, but disrupt the reproduction of individuals and groups (or, for example, promote the preservation, dispersal, and reproduction of groups, but at the same time disrupt the reproduction of genes and individuals).

Happy New Year, 2014, dear readers!

Column for Kompyuterra #130 Column for Kompyuterra #131 Column for Kompyuterra #132