Black Queen Rule. The black queen hypothesis may explain the extinction of land mammals

Is it true that the queen of evolutionary problems is the Red (a.k.a. Black) Queen? Don't rush to answer - don't forget about hermaphrodites!

Even for us humans, with all our ability to foresee events, it is not so easy to act in the interests of our own immediate descendants: remember the destruction of forests, global warming and the problem of overpopulation. How then, with her blindness and selfishness, could she put the long-term benefit of sex for the population above its short-term double price with all the ensuing unpleasant consequences? (Nick Lane. The Ladder of Life)

I am going to discuss in some detail the problem of the evolution of population reproduction and recombination (including the phenomenon of sex). Of course, all the key thoughts can be summarized in one short text, but at the same time they will turn out to be declarative and incomprehensible. To justify them, a text larger than an entire column is needed, but such a justification will be incomprehensible to non-specialists. I am trying to present both a complex set of well-known ideas and my own developments in such a way that they are understandable to thoughtful non-biologist readers. How to encourage such readers to understand the subject under discussion? For me, I often find interesting material about branches of knowledge that are unfamiliar to me, in which the logic of reasoning of the people developing these fields is visible. This is the logic I am trying to reflect, to the best of my ability and understanding of the material, in these columns. Naturally, the volume of text required for this is growing by leaps and bounds. This column is already the fifth in the “sex” series; there will be three or four more.

But do these experiments explain the origins of sex? Authorities such as Alexander Markov or Matt Ridley agree that the Red Queen explained the phenomenon of gender. However, they say that Alexander Kondrashov (the author of the Kondrashov ax mentioned in the last column) continues to consider the phenomenon of gender to have never received its explanation.

The experiments that Naimark writes about are undoubtedly convincing. However, do not forget: they cannot prove that the “strength” of the Red Queen would be enough to overcome the double drop in fertility caused by the transition from clonality to dioecy at the time of the origin of sexual reproduction.

When Caenorhabditis elegans we are dealing with a species in which sexual reproduction is already perfectly formed. The fact that in hermaphrodites it is degenerated due to self-fertilization is a secondary effect. By the way, when analyzing the described experiment, one must keep in mind that the descendants formed as a result of self-fertilization turn out to be more or less homozygous (having identical alleles), and the worms resulting from the crossing of males and hermaphrodites turn out to be much more heterozygous (they have different versions of homologous alleles). Increased heterozygosity can contribute to increased resistance on its own, without taking into account the consequences of recombination.

Anyway Caenorhabditis produces both eggs and sperm. The haplo-diploid life cycle with fertilization and meiosis is fully formed in these worms. The Red Queen can increase the proportion of worms with sexual development. At the same time, I doubt that it could ensure the evolution from clonal reproduction to sexual reproduction, overcoming a twofold loss in reproductive efficiency.

Now I have a confession to make. As I wrote in the column before last, I have my own version of the solution, I just took my time to explain it. In order for you to appreciate the way out of a theoretical impasse, you had to be led into this impasse. Even in this column I won’t have time to give all the rationale for the decision, but I can outline it.

The insightful (jokes aside) Nick Lane, quoted in the epigraph, does not share sex and its “double price”. He is not right. The decrease in reproductive efficiency is not associated with sexual reproduction as such, but with the presence of males who themselves do not leave offspring. What John Maynard Smith called the "double price of sex" might properly be called the "double price of dioeciousness." Hermaphrodites don't pay this price!

Let me remind you of the illustration that I gave when starting the conversation about the evolution of recombination.

In my distant childhood, I had a friend (and still have one), and at that time she also had a father who was a scientist, a nuclear physicist. My friend’s dad’s favorite fairy tale from our childhood was the fairy tale about Alice by Lewis Carroll. We didn’t understand him very well then, and we also really misunderstood the fairy tale - maybe it was the usual Cinderella and Little Red Riding Hood thing.

Now I, having grown up significantly and even a little wiser, have learned that the fairy tale about Alice is not so simple and not at all maddening, but quite the opposite. And it was written not just by some English storyteller Lewis Carroll, but by Oxford University mathematics professor Charles Lutwidge Dodgson (Carroll is a pseudonym). My friend’s dad, having extensive knowledge in physics and mathematics, understood the beauty of the encrypted laws of our world in the behavior of the heroes of Alice’s imaginary world.

Richard Dawkins, an English ethologist and evolutionary biologist, called this principle the “evolutionary arms race.”

Ecologists Robert MacArthur and Edward O. Wilson based their law on the same Black Queen effect, and formulated it in the book “The Theory of Island Biogeography.” In short: animals of species A are thrown onto a certain island by fate. Upon arrival in a new life, the species will most likely die out, but in order to survive (as well as quickly adapt), species A must actively reproduce, populating the newly acquired land. If the next species B is brought to this island, then it will need to adapt not only to the new life, but also to species A. As the number of animal species on the island increases, the number of extinct ones will increase. Over time, new arrivals will increasingly discover their own species on the island, which means the number of animal species will not increase, but extinction will also stop. If we plot the dependence of the rate of settlement (i.e., the number of new species arriving in a given period of time) on the number of species that have already inhabited the island, it is noticeable that the rate of settlement is high when the number of inhabitants of the island is small, and low when their number great. This MacArthur-Wilson equilibrium law can be easily applied to the theory of human settlement of cities.

An analysis of the processes of speciation and extinction of species, carried out on paleontological remains for 19 families of Cenozoic mammals, showed the validity of the Red Queen hypothesis, according to which the main cause of extinction was a gradual deterioration in the quality of the environment for the evolving clade (group of related species). The diversity of the entire group declines equally due to a decrease in the rate of speciation and an increase in the rate of species extinction.

The extinction of species, as well as their emergence in the process of evolution, occurs constantly, although the public's attention is more attracted to mass extinctions, the events themselves are quite rare. To explain the constant (background) rate of extinction of species, biologists are increasingly turning to the “Red Queen hypothesis” proposed by paleontologist Leigh Van Valen; see: L. M. Van Valen, 1973. A new evolutionary law (PDF, 2 MB). This hypothesis takes us back to “Through the Looking-Glass,” to the place in this unusual fairy tale by Lewis Carroll where the Red Queen makes Alice run faster and faster. When they finally sit down to rest under a tree, the out of breath Alice is surprised to discover that they have remained in the same place. The Queen explains that to run further, you need to run even faster. And when Alice says that everything is wrong in their country, the queen remarks, not without malice: “A slow sort of country!” (“Some kind of slow country!”):

Alice looked round her in great surprise.

“Why, I do believe we"ve been under this tree all the time! Everything"s just as it was!”

“Of course it is,” said the Queen: “what would you have it?”

“Well, in our country,” said Alice, still panting a little, “you"d generally get to somewhere else - if you ran very fast for a long time, as we"ve been doing.”

“A slow sort of country!” said the Queen. “Now, here, you see, it takes all the running you can do, to keep in the same place. If you want to get somewhere else, you must run at least twice as fast as that!”

Alice looked around in amazement.

What is this? - she asked. - We remained under this tree! Have we really not moved a single step?

Well, of course not,” answered the Queen. - What did you want?

U us“,” said Alice, hardly catching her breath, “when you run as fast as you can for a long time, you will certainly end up in another place.”

What a slow country! - said the Queen. - Well and Here, you know, you have to run as fast as you can just to stay in the same place! If you want to get to another place, then you need to run at least twice as fast!

(Translation by N. Demurova)

Our biosphere, however, is not a slow country. The evolution of living beings taking place in it also cannot stop, since the environment is constantly changing. If some organisms slow down the rate of evolution and no longer adapt to a rapidly changing environment, they simply die out. In the process of natural selection, through classical Darwinian evolution, new species arise that are better suited to new conditions.

The term comes from Lewis Carroll's Alice Through the Looking Glass, from Alice's dialogue with the Black Queen:

“With us,” said Alice, hardly catching her breath, “when you run as fast as you can for a long time, you will certainly end up in another place.

What a slow country! - cried the Queen. - Well, here, you know, you have to run as fast as you can just to stay in the same place.

Translation by N. Demurova

Arms race

The gender paradox and its meaning

Science author Matt Ridley popularized the term "Black Queen Effect" by linking it to sexual selection in his book The Red Queen: Sex and the Evolution of Human Nature(1993), in Russian translation - “Sex and the evolution of human nature” (2011).

In bisexual populations of living beings, males, making up, as a rule, about half of the population, do not have the opportunity to directly produce offspring without the participation of the female sex (if they do not have the biological ability to change their sex). In some species, such as lions, it is the custom among males to kill the young sired by another male (according to Richard Dawkins, this is a manifestation of the so-called selfish gene, whose purpose is only to reproduce, and which can consequently suppress the reproduction of other genes ). In addition, males and females must expend resources to attract and compete for the opposite sex. Sexual selection can also produce traits that reduce the fitness of the species and individual for survival, such that the brightly colored plumage of birds of paradise, used to attract a mate, at the same time increases the likelihood of being noticed by potential predators. Thus, sexual reproduction can be very ineffective in terms of the struggle for existence.

A possible explanation for the fact that almost all vertebrates are dioecious is that sex increases the ability to adapt. First, if a beneficial mutation occurs among asexually reproducing individuals, there is no way for that mutation to spread and for individuals to acquire genes from other lines of their species that may have developed their own beneficial mutations. Secondly, it shuffles the alleles. Some cases of hereditary variation could only be advantageous when one mutation combined with another mutation, and sexual reproduction increases the likelihood that such a connection will occur.