This article is from the magazine Les Indispensables de Sciences et Avenir n°210 dated July/September 2022.
From the porcupine urinating on its companion to induce ovulation to the echidna equipped with an improbable phallus with four acorns, passing through the marsupials Antechinus frantically reproducing until they die of exhaustion, the animal world is full of an incredible diversity of strategies, behaviors and sexual organs, each stranger than the next. But why such exuberance when it comes to getting together?
An evolution of gametes
In reality, there was a time when the thing was very simple. More than a billion years ago, sexual reproduction resulted from the encounter between two strictly identical gametes. Until some organisms start making smaller gametes, thus benefiting from a big evolutionary boost: the production of each gamete requiring less energy, it becomes possible to make many more and therefore obtain potentially larger offspring. On condition, however, that these small gametes, less rich in nutritional resources for the future embryo, merge with larger ones which will compensate for this deficit.
A few hundred million years of evolution later, these two strategies pushed to their climax have become the norm in animals. “This is the very definition of males and females: the first having small mobile gametes, spermatozoa, the second producing large nutritious gametes, oocytes, recalls Sylvain Billiard, lecturer at the University of Lille. This will lead the two sexes towards very different reproductive strategies, behaviors and even morphologies.”
Thus, while males with innumerable gametes will rather seek to multiply conquests, adorning themselves with seductive trappings, females will tend to bet on quality by providing the resources necessary for the development and survival of their offspring. In terms of sexual dimorphism, some animals have pushed this partitioning of roles so far that males and females seem to belong to totally different species.
In marine worms of the genus Osedax, for example, the males are several tens of thousands of times smaller than the females and live inside the latter, constituting a veritable harem of a hundred microscopic lovers. Still in the depths, the difference in size between the two sexes in the abyssal anglerfish is not as spectacular (the male is only five times smaller), but the species compensates with another strangeness: when a male meets his gigantic companion, he bites her without ever opening his jaw again. Over time, his skin and his blood system merge with those of his sweetheart, his organs that have become useless (eyes, fins, etc.) disappear. In the end, all that remains is a simple pocket of flesh that provides spermatozoa, clinging to the female.
The intensity of the color of the legs, a criterion for choosing a partner
This type of behavior, and more generally the fact of delegating most of the costs of reproduction to the female (the initial nutrient supply of the gametes, but also the suckling and rearing of the young, etc.), has prompted certain biologists to speak of real “parasitism of the male”, which transmits its genetic heritage without undergoing the disadvantages of reproduction. In addition to the anglerfish of the abyss, the term takes on its full meaning in the Zeus bugs, whose male takes up residence on its companion. The unscrupulous thus allows himself to be transported for weeks while feeding on a substance secreted by his partner’s back.
With reproduction much more costly for the female, who also has a limited number of gametes, she has every interest in choosing the best father for her offspring – the one whose genes will guarantee the best chances of survival. The selection criteria are sometimes most surprising. In the Pacific, female blue-footed boobies base themselves on the intensity of the color of the legs of their aspirants. In Australia, the satin gardener is judged on his talents as a builder: to convince his beauty, this bird builds a monumental arch made from intertwined twigs, which he paints with a piece of bark brushed with crushed berries. . On the island of New Guinea, male birds of paradise engage in courtship displays that are as complex as they are endless. The prize goes to Carola’s bird-of-paradise, of which an American ornithologist has identified no less than fifty-eight dance elements arranged in twenty distinct sequences.
A phallus without an orifice whose sole role would be to give pleasure
Finally, still among birds, the red-billed alecto female could well choose her lovers according to the pleasure they give her. While most birds lack penises, simply copulating vent to vent, this African passerine bird appears to have one…in appearance only. This pseudo-phallus not having any orifice, its only role seems to be to give pleasure. The males endowed with a longer organ than the others find themselves in any case at the head of a harem.
“It’s all these choices made by females that drive evolution.says Thierry Lodé, professor of evolutionary ecology at Rennes-I University. On the side of the males, the objective will on the contrary be to limit this selection by developing strategies to circumvent their choice. For many species, this bypass will not be smooth. In bed bugs, the male simply pierces the female’s shell at random to inject his semen. In ducks, males will also impose themselves mainly by rape, well helped in some species by an oversized penis (the record is 42 centimeters!) capable of “explosive” erections, unfolding in less than half a -second inside the female. “In response, this one has developed a vagina forming a real labyrinth, which she could control in order to let the sperm pass or not, and finally choose which male will fertilize her”describes Thierry Lodé.
Bruchids, small beetles that seem quite innocent at first sight, offer another example of this arms race between the two sexes. The males have an eminently destructive reproductive organ, a kind of medieval mass covered with sharp spikes. This shape could both help them hold the female in place and promote the release of sperm. If the females have evolved in return to a reinforced reproductive system to limit breakage, many are seriously injured by these penetrations, sometimes until death.
For a male, succeeding in copulation is also only a first step towards reproduction: he must also ensure that he will indeed be the father of the future offspring. In many insects, molluscs and spiders, the females have spermathecae, organs that store spermatozoa, where the contributions of the different lovers are diluted. Before copulating, the male dragonfly therefore firmly seizes his companion using abdominal clamps and undertakes to meticulously clean the spermatheca via his penis, removing the sperm already present. In many species (rodents, reptiles, worms, etc.), the male will prefer to leave a “copulatory plug” in the female reproductive system, a dense substance that will block the passage to the next male.
Faced with such competition, such a fierce struggle between the two sexes, hermaphroditism seems to be a more serene way of considering reproduction, with moreover some non-negligible advantages. “This already doubles the chances of reproduction, since it becomes possible to mate with any partner, even to self-fertilize”, describes Patrice David, director of research at the Center for Evolutionary Functional Ecology. The researcher and his team have however shown experimentally that such self-fertilization ends up reducing genetic diversity and therefore adaptation to the environment.
But even in hermaphroditic species, the conflict between males and females is never far away, as illustrated Pseudoceros bifurcus. When two of these nudibranchs meet, a real duel is played out with great blows of reproductive organs, each trying to penetrate the other first before fleeing, leaving the loser the joys of motherhood. A sexual conflict that is also found in successive hermaphrodites, who change sex during their existence. While some, like the green goby, make their transition after finding a soul mate, to ensure that they form a fertile heterosexual couple, others make more tactical choices. “When there is very strong competition between males, some hermaphroditic fish prefer to remain female until they are strong enough to compete, or until the dominant male finds himself in a bad position”describes Patrice David.
If hermaphroditism seems to have so many advantages, why isn’t it more widespread in the animal world? “That’s a good question, to which we don’t really have an answer! laughs Sylvain Billiard. In reality, natural selection will never favor a single strategy, several can even coexist within the same species. Enough to offer a whole range of sexual practices to make naturalists blush.
Female penises, giant sperm…
It is an immutable rule in zoology: no rule is immutable. Particularly when it comes to reproduction, because the living world is full of counterexamples and exceptions. Male gametes are by definition very small? Talk to the fly Drosophila bifurca, whose male measuring barely 3 millimeters produces sperm of 6 centimeters each. During copulation, these giant spermatozoa pass through a genital structure that rolls them up like a ball of wool and sends them one by one inside the female.
The males multiply the conquests, leaving the breeding of the young to the females? The counter-examples of “good fathers” are legion, from the seahorse to the midwife toad, without however equaling the black jacana. This South American bird radically reverses the roles: the females fight among themselves to obtain the favors of the males, then leaving the latter to take care of the brooding and then the education of the young. Finally, insects of the genus Neotrogla also reverse the roles, but from a morphological point of view this time. Females are endowed with a furiously penis-like organ that they use to penetrate males for up to 70 hours, in order to suck their sperm through this curious female phallus.
By Yann Chavance