On the Nature of Male and Female, or From Conjugation to Oogamy. Column for Kompyuterra #138

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Dmytro Shabanov
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Discussion of the Transition from Hermaphroditism to Separate Sexes as an Example of Non-Classical Development of a Natural Science Hypothesis On the Nature of Male and Female, or From Conjugation to Oogamy Unwritten Column. On Violence: A Simple Ethical Problem and an Analysis of Three Examples from Modern Ukrainian Life

Column for Kompyuterra #137 Column for Kompyuterra #138

I am continuing the series of "sex" columns, or more precisely — columns on the evolution of recombination. This one is already the eighth in order, and here is the first). After explaining why I hypothesize that sexual reproduction could have originated in hermaphrodites, I want to discuss a theory that creates serious problems for such views. I was asked why I was "silent" (not writing new columns) for two weeks. I couldn't figure out in my mind how what I will present here combines with what I wrote before. The question remains open for me. The solution I found is this: here I will present the facts that are significant to me, which will make the diversity of forms of the sexual process more understandable for readers, and I will postpone the main conclusions I am trying to formulate. I will begin with truths of the kind presented in textbooks. The sexual process is associated with fertilization — the fusion of hereditary material from two cells. As I wrote in the second column from the "sex series," in a typical case fertilization consists of two stages — the fusion of two cells (syngamy) and the fusion of their nuclei (karyogamy). What are these cells that fuse? They can be unspecialized cells representing part of the body or the entire body of a unicellular organism — and this case can be called somatogamy. Most often the concept of "somatogamy" is applied only to fungi, where cells from different hyphae can connect, but in a broader sense it can be applied to many other cases where cells that perform other functions are used for fertilization. In this broad interpretation, conjugation is the most common type of somatogamy. In it, the cells of two organisms (unicellular or multicellular) connect through bridges, through which migrating nuclei are transmitted (sometimes — together with all the cell contents). During conjugation, information can be transmitted in both directions (for example, in the ciliate Paramecium) or only in one direction (for example, in the alga Spirogyra). Naturally, the first case is analogous to cross-fertilizing hermaphroditism, and the second — to gonochorism. [IMG_1] This is how conjugation occurs in some algae (figure from the classic reference "Life of Plants") Conjugation (and other forms of somatogamy in the broad sense) seems primitive and archaic to you? Let me tell you how it occurs in the most complex cells, in terms of their structure, created by Earth's evolution. I am talking about the most highly organized unicellular organisms — about ciliates, such as the "school" ciliate Paramecium. Ciliates reproduce (divide) by pinching in half along their long axis. And during conjugation, two ciliates press against each other along their long sides. [IMG_2] Reproduction (left) and conjugation (right) in Paramecium Reproduction occurs without the sexual process, and the sexual process occurs without reproduction. The other thing is that after the sexual process, ciliates become, in essence, new individuals that subsequently proceed to division — clonal reproduction. Surprisingly, a clone consisting of many generations of cells passes through stages of immaturity, maturation, maturity, and old age. After the end of the immaturity period (during which a certain number of generations of cells reproducing by division succeed each other; in Paramecium it lasts about a month) the clone becomes capable of conjugation. It is possible with genetically different clones that belong to another mating type (some kind of sex analogue). The number of mating types in different ciliates can vary: 2, 4, 6, 7, 8, 10... The trigger for transitioning to the sexual process can be a deterioration (from the ciliate's point of view) of living conditions. As long as everything is going well, ciliates divide, preserving the genotype appropriate (since for its possessor everything is going well) to the living conditions. However, if a ciliate has divided hundreds of times and has not undergone sexual "renewal" during this time, then over time it loses the ability to divide further and dies. Imagine: a culture is growing and developing an aging clone of ciliates. Since all individuals belong to one clone, they also have one mating type. Starting from some time, the entire experimental population is doomed: the individuals composing it cannot find partners for the sexual process. The clone has aged: ciliates live, divide, but regardless of how events develop, after a certain number of generations their reproduction will stop... Paradox? Certainly. Here some mechanism manifests itself that prevents ciliates from abandoning the periodic sexual process. The ciliate cell is very complex, and the genes necessary for its vital activity are multiplied many times in one of the two nuclei of the ciliate — the large nucleus, the macronucleus. Before conjugation, the macronucleus is destroyed, and the micronucleus, the small nucleus, undergoes meiosis, dividing into four unique nuclei with half the amount of genetic information. Three of the four nuclei die, and one more divides once more by means of mitosis, forming a stationary ("female") and a migrating ("male") nucleus. The two ciliates exchange migrating nuclei, which fuse with the stationary nuclei of the partner ciliate, forming new micronuclei. As a result, two genetically identical exconjugant individuals are obtained... Why did I spend so much space discussing the case of ciliates? It shows that reproduction without the formation of specific cells can be used by extremely highly organized beings. Moreover, in their example, the connection between the sexual process and the phenomenon of death is traced. Believe me, although this connection is insufficiently realized, it is quite profound. Without spending time on its justification for now, I will express an important idea: the causes that ensure the sexual process are closely related to the causes that ensure the programmed death of individuals... Let us proceed to the second, much more widespread type of the sexual process — with the use of specialized sex cells, gametes. This type of sexual process is called gametogamy. Gametes can be produced by both unicellular and multicellular organisms. Three main forms of gametogamy are known. In isogamy, the gametes that fuse with each other have the same size. These are motile cells that intensively search for each other. These cells can be completely identical externally, but they nevertheless carry biochemical markers that ensure the fusion (syngamy) of different cells. One cannot speak of sex here; different types of gametes can be denoted, for example, by the signs "+" and "—". In anisogamy, the motile gametes turn out to belong to two types — large and small. In this case, it is understandable that large gametes correspond to the female sex, and small ones to the male. The logical conclusion of this evolution is oogamy. The female gamete loses active motility and is called an egg cell; its search is the task of small and motile gametes, which are called spermatozoa. [IMG_3] Comparison of three forms of gametogamy and conjugation ("Life of Plants") Probably the simplest variant of gametogamy is isogamy. As it seems, this method of reproduction is the most "logical" and simple. Why then do we observe oogamy in most highly organized species? Recall the column in which I told about the possible mechanism of transition from hermaphroditism to gonochorism. The success of one or another solution depends not on its optimality, but on its stability (or instability). Isogamy turns out to be unstable. The possibility of such a mechanism of transition from isogamy to anisogamy, about which I will speak, has been recognized for a long time. The first publication on this dates to 1972 (Parker, G. A., Baker, R. R. and Smith, V. G. F. The origin and evolution of gamete dimorphism and the male-female phenomenon. Journal for Theoretical Biology, 1972, v. 36, p. 529–553). This concept is usually called the PBS theory, after the first letters of the surnames of its three authors. Since the creation of this theory, modeling the interaction of gametes of different sizes has become a separate branch of science. I will describe the main idea, using my own model, much more primitive than the best examples created for studying this problem. The model can be downloaded from my website: either the version for Excel-2013, which I worked with, or a slightly simplified version for Excel-2003. Let us consider a population of organisms that release gametes into the water. The initial state is typical isogamy. Organisms belonging to both mating types (1 and 2) produce gametes of the same size. In the case shown in the figure, the size of all gametes is 12.5% of the maximum possible. Gametes meet in the water column, fuse, and form a zygote. With a probability of 50%, the individual belongs to the first or second type. It will produce gametes of the same size as its parent belonging to its mating type, with a small clarification. With a small probability d (in the shown example d=0.005), the individual switches to producing gametes of the neighboring size class: twice as large or twice as small. All individuals invest the same amount of energy in gamete production, and therefore those individuals that produce gametes twice as small will release twice as many of them into the water. The last thing that needs to be explained before discussing the results is that the probability of zygote survival depends on the amount of energy they received from the gametes (simply from their size). The simplest variant of the dependence is direct proportionality between zygote size and its chances of survival. Let us see what happens. [IMG_4] A window with a brief description of the model, cells for entering initial parameters, and the final graph of its operation. Gametes of the first sex are shown by a solid line, of the second — by a broken line. Zygote survival is directly proportional to their energy reserve. In the initial state, both types of organisms produce gametes at 12.5% of maximum; by the end of the simulation, the first type produces exclusively gametes at 1.6%, and the second — mainly at 6.3% of maximum Both "sexes" reduce the size of their gametes. Why — is easy to understand. With the constant size of the partner's sex cells, the individual that reduces its gametes by half will double the number of its offspring, and their survival will decrease by only 75% (the energy reserve of the zygote depends on the size of both gametes). In this situation, both "sexes" reduce the size of their sex cells. This occurs to the limit at which zygote survival becomes dangerously low. Are the conditions I used realistic? Not entirely. Probably a zygote that is smaller than some minimum size has no chance of survival at all. The viability of a zygote in such a case should be proportional to the difference between its size and this minimum. [IMG_5] Two variants of the dependence of zygote survival chances on its size (determined by gamete size) It is worth switching from the first variant of the dependence of zygote survival chances to the second, and the behavior of the model changes dramatically. Increasing gamete size also turns out to be a profitable strategy (look closely: the events in the picture below begin with the "sex" shown by the dotted line switching to producing larger sex cells). [IMG_6] Here the second variant of the dependence of zygote survival chances on its size is implemented. At the beginning of the simulation, both sexes produce gametes at 12.5% of maximum; by the end (after 128 generations), the first sex gives almost exclusively gametes at 0.8%, and the second — at 100% of maximum size Under these conditions, the model quickly transitions to a state where one sex produces the largest possible gametes, and the second — the smallest. Which particular sex turns out to be "large-gamete" and which — "small-gamete" is decided by chance. As you see, in our model we observed the transition from isogamy to anisogamy. As I already said, much more sophisticated models have been developed for studying this transition, which also take into account other factors. For example, it is obvious that the probability of gamete meeting depends on the efficiency of their swimming, which, in turn, depends on their sizes (in particular, affecting the Reynolds number — a value that determines the nature of the fluid flow around the gamete). Taking such factors into account leads to more complex dependencies, which, nevertheless, confirm the general pattern: isogamy is relatively unstable and is very likely displaced by anisogamy. [IMG_7] Three-dimensional visualization of the results of much more complex modeling. The height of the peaks reflects the stability of various combinations of gamete sizes. Isogamy corresponds to a small peak in the middle, and anisogamy — to two symmetrically located higher peaks at the edges (from the book: T. Togashi and P. A. Cox (editors). The Evolution of Anisogamy. Cambridge University Press, 2011, 250 p.) And do you know what we got in the end? Gonochorism! The thing is that males are the sex that produces many small sex cells, and females are the sex that produces few large ones. All other discrepancies between females and males are consequences of this primary difference!

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Dmytro Shabanov
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Discussion of the Transition from Hermaphroditism to Separate Sexes as an Example of Non-Classical Development of a Natural Science Hypothesis On the Nature of Male and Female, or From Conjugation to Oogamy Unwritten Column. On Violence: A Simple Ethical Problem and an Analysis of Three Examples from Modern Ukrainian Life

Column for Kompyuterra #137 Column for Kompyuterra #138