Are Eight Indirect Hypotheses Describing the Advantages of Sexual Reproduction Sufficient to Explain the Origin of Sex? Column for Computerra #133

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Dmytro Shabanov
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Column for Computerra #132 Column for Computerra #133 Column for Computerra #134

The paradoxical nature of sexual reproduction, discussed in my previous column, is such that some readers were unable to grasp it. Consider: in sexual reproduction, any gene of an individual is transmitted to offspring with only a 50% probability, whereas in various forms of clonal reproduction the probability is 100%! Let us once again examine the scenario that most authors discuss. A species with clonal reproduction transitions to sexual reproduction (with males and females). As John Maynard Smith correctly noted, such a transition can be justified only by a twofold greater survival rate of offspring from sexual reproduction, and immediately, in the short term. This is most easily demonstrated with a table. Imagine a population divided into two subpopulations (parts), A and B, differing in their mode of reproduction (a classification of reproduction types was given in that column). "Competition" 1 Mode of reproduction

Parents Offspring

Survival rate Survivors

Total

Result

Subpopulation A

Clonality (type I)

Total

Result

Individual 1 100

25% 25 50 Loss Individual 2

100 25 Subpopulation B

100

25 %

25

50

Loss

Gonochorism (type III)

100

25

Subpopulation B

Female 100 51% 51 51 Victory Male — In the competition shown, subpopulation B will displace all members of subpopulation A within a relatively small number of generations. Note, however, that the victory of sexual reproduction in this case is associated with an incredible, more-than-twofold increase in offspring survival (the probability for offspring to reach some comparable stage in their life history). Such a rapid increase in survival must be associated with some extraordinarily substantial advantage! Could this really be nothing more than a reshuffling of genes? What if the survival gain falls even slightly short? Let us look.

Female

100

51 %

51

51

Victory

Samec'

—

"Competition" 2

Mode of reproduction

Parents

Offspring

Survival rate

Survivors

Total

Result

Subpopulation A

Clonality (type I)

Individual 1

100 25% 25 50

100

25 %

25

50

Victory Individual 2

Individual 2

100

25

100 25 Subpopulation C

Gonochorism (type III) Female

100 49%

100

49 %

49

49

49 49 Loss

Male —

—

If the survival advantage of offspring falls short of twofold, clonal organisms displace gonochoristic ones in the short term. The long-term advantages of sexual reproduction simply do not have time to manifest in such a situation! But why is sexual reproduction so widespread? This requires a special explanation, and in this column I shall describe its various versions. You will recall, I hope, the "Vicar of Bray" mentioned last time. Dawkins's hypothesis of the "selfish sex gene" — the version that readers of the past three columns mentioned most frequently. "The difficulties theorists face in explaining the evolution of sex are at least partly due to their assumption that the individual strives to maximize the number of its surviving genes. In light of this assumption, sexual reproduction appears paradoxical. <...> However, this paradox will seem less paradoxical if, in accordance with the arguments in my book, we regard the individual as a survival machine created by a short-lived confederation of long-lived genes. <...> If sexual reproduction, as opposed to asexual reproduction, is advantageous for the gene that determines sexual reproduction, that is sufficient to explain the existence of the latter. Whether it is advantageous for all the other genes of that individual is not very important. From the standpoint of the selfish gene, sexual reproduction is not such a strange phenomenon at all." Richard Dawkins. The Selfish Gene To correctly understand Dawkins, one must clarify what he means by "gene." "...there is no universally accepted definition of a gene. <...> I wish to use a definition due to G. C. Williams: a gene is any portion of chromosomal material that potentially lasts for enough generations to serve as a unit of natural selection. <...> A gene is a replicator with high copying fidelity." Richard Dawkins. The Selfish Gene I would not, of course, tie the concept of "natural selection" so unambiguously to the level of genes... Preserving the meaning, Dawkins's approach can be expressed as follows: a gene is a fragment of genetic text that is transmitted from generation to generation as a single unit (which does not preclude the possibility of its change). Let us ask whether a "gene for sexual reproduction" exists as a single entity. No! In the column before last, I deliberately spent considerable effort explaining that sexual reproduction is a phenomenon linked to the haplo-diploid life cycle with fertilization and meiosis. This evolutionary invention brought together mechanisms of homologous recombination perfected in meiosis, as well as systems ensuring syngamy and karyogamy (these terms are explained in that column). To explain the origin of sexual reproduction as the origin of some "gene" that suddenly acquired such an effect is to believe in a fairy tale. Does this mean Dawkins's explanation is entirely wrong? Not that either. Recall (again from the column before last) the infectious transmission of "sex" in bacteria. Escherichia coli harboring a small circular DNA molecule called the F-factor thereby acquires the ability to form pili (structures for DNA injection) and to transmit to other bacteria both the F-factor and other DNA fragments. A "sexual" individual infects an asexual one with "sex" by inserting a pilus into it. In this case, Dawkins's explanation proves at least quite workable. In organisms possessing a haplo-diploid life cycle with fertilization and meiosis, the very readiness of an individual for reproduction is the result of coordinated action by many independently arisen and evolved genes, each of which faces a 50% probability of not passing to the next generation. A "selfish sex gene" simply does not exist in such organisms! So what is the advantage that ensured the triumph of sexual reproduction? A number of hypotheses have been proposed on this subject, and I wish to briefly describe several of them. These hypotheses are characterized in greater detail in Matt Ridley's "The Red Queen," in Vigen Geodakyan's book "Two Sexes. Why and What For?", and also in articles by K. Yu. Popadyin and I. A. Rukhlenko. Muller's Ratchet. Hermann Muller drew attention to the fact that in clonal transmission of genomes, errors arising in them — mutations — can be corrected only through the death or reproductive exclusion of their carriers. If carriers of error-free genotypes disappear due to the mutational process or simply by chance, the "cleanest" genotypes will be those carrying a single mutation. This situation may persist for some time, but sooner or later it will inevitably end with the random disappearance of genotypes carrying one mutation. Then the best genotypes will be those with two mutations. An "error-free" genotype can never be restored. This continuous deterioration of clonal genomes is reminiscent of a ratchet — a toothed wheel that can only tighten handcuffs, never loosen them. [IMG_1] Left — Hermann Joseph Muller (1890–1967). Right — a ratchet: a toothed wheel that can rotate in only one direction (in the case shown in the figure, clockwise) Muller's Ratchet, for example, accounts for the degeneration of the human Y chromosome, and the reason for this is precisely that it is transmitted from generation to generation clonally. The hypothesis associated with this mechanism holds that it limits the viability of clonal species, creating advantages for sexual ones. As a result of Muller's Ratchet, the overwhelming majority of species that have abandoned recombination are, broadly speaking, doomed. Those with relatively small genomes, high population numbers, and effective selective control go extinct more slowly, but their prospects are nonetheless bleak. Progressive evolution prior to the origin of sexual reproduction was ensured by other forms of recombination, while after the origin of sex, both the development and the mere maintenance of a functional genotype became linked to it. Consider: when organisms each carrying a single deleterious mutation interbreed, one quarter of their offspring will inherit neither mutation! Nanney's Hypothesis is a development of the Muller's Ratchet idea. L. Nanney proposed that all species with sexual reproduction in whose evolution asexual clones arose were displaced by those clones and went extinct, and later (as a result of Muller's Ratchet) those clones also went extinct. Therefore, through group selection, only such sexually reproducing species survived as had, for some reason, lost the ability to transition to clonal reproduction. What then of the daphniids that abandon the sexual process, which I described in the previous column? From the standpoint of Nanney's Hypothesis they are halfway to extinction... "Kondrashov's Hatchet" — Kondrashov's mutational deterministic hypothesis. Proposed by the Russian (now Russian-American) biologist Alexei Simonovich Kondrashov. This hypothesis draws attention to how weakly deleterious mutations, individually, are distributed in a population of sexually reproducing organisms. Some individuals carry a small number of such mutations, others carry many. Suppose the effects of these mutations are synergistic: the more there are, the lower the individual's viability. Consider the distribution of individuals by the number of mutations they carry. Selection will cut off, like a hatchet, the most heavily loaded classes of individuals, simply removing the "tail" of the distribution. Each death of an individual from these distribution classes removes many mutations from the population gene pool; in asexual organisms, equivalent purging would require the death of many more individuals. In addition, Kondrashov drew attention to the evolutionary consequences of the alternation of haploidy and diploidy discussed in the previous installment. A lethal mutation in a haploid organism leads to its death. A diploid organism may carry several lethal mutations across its two chromosome sets and remain perfectly viable. On the other hand, genes that cause death at the haploid phase (either in a separate haploid generation or at least in haploid gametes) will be efficiently eliminated from the population, being prevented from reaching the diploid phase. Unlike the "Vicar of Bray" and Muller's Ratchet, Kondrashov's hypothesis concerns the short-term advantages of organisms arising from the sexual process. Manning's Sexual Selection Hypothesis. The English biologist John Manning draws attention to the fact that females, when choosing males, are capable of conducting a sufficiently effective assessment of male fitness. This has been demonstrated for humans and for many other animals — those, however, characterized by complex behavior. There is no reason to doubt that this mechanism operates in many cases. On the other hand, this hypothesis does not explain the transition to sexual reproduction from clonal reproduction, when the refined mechanisms of sexual selection had not yet arisen. I would call Geodakyan's "Evolutionary Theory of Sex" the informational hypothesis of Geodakyan. The Russian physicist and geneticist Vigen Geodakyan put forward a number of original ideas concerning how information about which genotypic features of individuals prove adaptive to the environment is reflected in a species' gene pool. He compellingly demonstrates that evolutionary novelties are tested primarily on males (on the representatives of the sex that is less costly to lose). Of course, Geodakyan's views deserve a separate and preferably detailed treatment. Here I will only say that, in my view, he has a whole series of good ideas, but also quite a few clearly questionable judgments. And, of course, I cannot agree with his overall self-assessment of his work. "The breadth of the theory, its explanatory and predictive potential, allow it to take the place of many partial and imperfect theories in the field of sex, in particular Darwin's theory of sexual selection." V. Geodakyan. Two Sexes. Why and What For. — P. 5. This column can accommodate only two more ecological hypotheses, concerning the short-term ecological advantages of organisms arising through sexual reproduction. Williams's Lottery Hypothesis appeals to me especially. For a simple reason: I had arrived at it myself earlier — and only afterwards read about it in Ridley and Geodakyan. I was thinking about exposure bracketing in photography. When a photographer does not know whether the exposure they have set suits the available lighting conditions and the characteristics of the subject, and when they need not economize on every frame, they can use bracketing. One frame is taken automatically with the settings currently on the camera, one with an exposure increased by one stop, one with it decreased. Exposure can only be increased or decreased, whereas for changing the properties of offspring there are many degrees of freedom. What should be changed? Those traits by which the parent (having passed through the crucible of selection) differs from its conspecifics, who are likewise "tested" by natural selection. At first glance, George Williams's hypothesis accords well with the analysis of life cycles. As long as conditions remain constant, daphniids and aphids reproduce clonally. When conditions change, a sexual generation appears, increasing the diversity of offspring. When a strawberry plant or a colony of coral polyps colonizes its immediate surroundings, it does so clonally: the strawberry sends out stolons, while corals bud. Distant habitats, however, are colonized by seeds or larvae produced through sexual reproduction. Organisms that seek sites for their offspring only at a distance (such as elms or oysters) rely exclusively on sexual reproduction. Unfortunately, analysis of the distribution of clonal and asexual forms is considered to refute Williams's hypothesis. According to it, one might expect that sexual reproduction would be more effective in harsh and variable environments, and asexual reproduction in favorable and stable ones. Yet it is known that asexual reproduction is more commonly adopted by species inhabiting extreme habitats. Bell's Tangled Bank Hypothesis — a development of the lottery hypothesis. Graham Bell proceeded from the observation that sexual reproduction is advantageous where offspring produced in excess compete primarily with one another. The more similar individuals are to each other, the more intense the competition among them; the carrying capacity of the environment for identical organisms is lower than for diverse ones. The name of this hypothesis alludes to the famous concluding passage of Darwin's On the Origin of Species. "It is interesting to contemplate a tangled bank, clothed with many plants of many kinds, with birds singing on the bushes, with various insects flitting about, with worms crawling through the damp earth, and to reflect that these elaborately constructed forms, so different from each other, and dependent upon each other in so complex a manner, have all been produced by laws acting around us." Charles Darwin. On the Origin of Species But the Tangled Bank Hypothesis accords poorly with the fact that the largest and most complex organisms, which often produce few offspring, reproduce almost exclusively sexually. Of the hypotheses explaining the advantages of sexual reproduction that I wished to describe, only one remains unmentioned — the one considered the frontrunner by many authoritative authors. This is Van Valen and Hamilton's Red Queen Hypothesis. It must be discussed in detail, and its treatment simply cannot fit into this column. Well then — next time. We shall see whether it can explain a discrete twofold increase in offspring survival... ← Dmitry Shabanov →

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Dmytro Shabanov
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The Queen of Problems in Evolutionary Biology: Jenkin's Nightmare Returns Are Eight Indirect Hypotheses Describing the Advantages of Sexual Reproduction Sufficient to Explain the Origin of Sex? Is it really true that the queen of evolutionary problems is the Red (a.k.a. Black) Queen? Do not rush to answer — do not forget about hermaphrodites!

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