How the birds have lost the phallus

Few organs are distinguished by such external diversity as the phalluses. In animals with internal fertilization, genitals are evolved quickly, their size and shape even in close species can vary significantly. Perhaps the most amazing animals in this regard are birds. In 3% of the species, the phalluses are long, flexible, diverse, but in the rest of 97% they are very reduced or completely absent. The absence of the external genitalia does not bother at all, but scientists have been racking their heads over the nature of this evolutionary incident.

The key to solving was found by the specialists of the Medical Institute of Howard Hughes and the University of Florida (USA) and English scientists from the University of Reading. It turned out that the lack of phallus in representatives of the reserve detachment is associated with the activation of cell death in the sex tubercle at a certain stage of embryonic development. Researchers note that in their work the latest achievements of phylogenetics, reproductive ecology and comparative morphology of birds, as well as the biology of the development of the genitals of mammals.

These achievements, in particular, allow you to follow how the birds parted with the phallus. In males of ancient Beskille birds (Paleggnathae), genitals are well developed, in representatives of the younger cubic detachment (AnteriFormes), too, and in most species of the nursing detachment (Galliforems), only the rudiment on the front wall of the cloak remained from the genital organ. The most evolutionarily new treasure of birds, NEOAVES, to which most living species belongs, is completely complete without a phallus.

Researchers compared the embryonic development of the genitals in the Seleznya of the Peking duck Anas Platyrhynchos, a representative of the goose -shaped detachment, and roosters of the Gallus Gallus Domesticus homemade chicken. For comparison as an external group, they studied the Bessile birds of EMU and the closest relative of birds, alligator. In both types, the laying of the sex tubercles occurs at the same stage of embryonic development. They develop in a similar way to a certain stage, after which the formation of the phallus in the roosters stops and the sex tubercle is resolved, while in the selezny embryo it continues to grow.

Genes regulating the growth of the sex tubercle are known. In both embryos, they work equally and absolutely normal. The cell reaction to the signals of growth factors is also not disturbed. But at a certain stage of development in the cocks, apoptosis of the cells on the tip of the sex tubercle begins, just at the time when its reduction occurs.

There is no morphogenesis without apoptosis. In the sex tubercle, he goes, but not very actively. In EMU, apoptosis of the sex tubercle cells is also weak, and in the aligator embryos, it is generally barely noticeable. And most importantly - none of these species apoptosis affects the tip of the tubercle. Researchers concluded that active cell apoptosis in this area is the evolutionary acquisition of reservoirs. But what could call him?

The first candidate is the family of bone morphogenetic proteins (Bone Morphogenetic Proteins - BMP). They got their name, since initially scientists discovered their ability to influence the formation of bones and cartilage, although in general these proteins regulate morphogenesis of different organs, including the sex tubercle (installed on mice).

Researchers compared the expression of BMP2, BMP4 and BMP7 genes in Selezny and Rooster embryos and found differences that occur at the stage of the previous regression of the future phallus. In the embryos of the Seleznya BMP4 and BMP7, they are expressed only in the cloak and at the base of the sex tubercle, in the cocks - along its entire length, including the tip, i.e. BMP gene expression coincides in space and time with a wave of death of the sex tubercle cells.

Scientists blocked the effect of BMP protein. They saturated porous acrylic balls with Noggin protein solution, which binds BMP and blocks its interaction with receptors. These balls with a diameter of 125-250 microns were applied on one side of the chicken embryo sex tubercle before it began to resolve. Noggin blocked the apoptosis of the cells for 24 hours, and the half of the sex tubercle, on which the balls lay, continued to grow. The difference in size turned out to be more than six times (100.8 microns versus 15.6 microns). Balls saturated with a neutral buffer did not affect apoptosis. And if you put the balls, soaked, BMP2 (analogue BMP4 ) on the sex tubercle of the duck embryo, they will cause apoptosis and the regression of the tubercle.

The researchers came to the conclusion that the activity of the BMP4 on the tip of the sex tubercle is necessary and sufficient for apoptosis and regression of the phallus in reservoirs. This activity arose in them during evolution.

To the question of how the birds lost the phallus, the scientists answered, but it remains incomprehensible what advantages this gives to the birds and why this strange sign has been preserved. So far, you can only guess about this, although there is, of course, hypotheses.

One of them is based on the fact that copulation with a male, devoid of genitals, is impossible without the active participation of the female. The partner cannot force her to sexual intercourse. Birds should accurately combine the holes of the clock, and the female turns the vagina. Thus, it controls paternity, i.e. The loss of the phallus helps to strengthen the role of a female in choosing a sexual partner.

According to an alternative point of view, the reduction of the phallus is a side result when selecting another sign. Genes regulating the development of the external genitalia also control the formation

limbs, intestines, nervous system, muscles and other structures. In particular, the BMP genes in certain tissues are also owe to a change in the loss of teeth, a variety of beaks and feathers. By the way, the rudiments of the teeth, as well as the first and last fingers, develop in bird embryos, but then resolve, as well as the sex tubercle. Perhaps BMP activity in the formation of different organs control the same genetic elements. But even if the radiation of the phallus is not the purpose of selection, but its side result, the further preservation of this feature requires constant stabilizing efforts.

As the authors of the work emphasize, the genetic mechanism for the formation of the phallus in birds is not disturbed, so theoretically it can turn from the rudimentary organ into a functional one. For this, the BMP4 gene activity is enough. Perhaps this is exactly what happened with Cracidae woody chickens, the owners of a completely functional phallus, although not as well developed as that of the cube -like ones.

Scientists intend to continue comparative studies. In particular, they are interested in which mechanism led to the complete gear of the phallus in Neoaves.

Herrera et al., Developmental basis of Phallus Reduction During Bird Evolution, Current Biology (2013), http://dx.doi.org/10.1016/j . Cub 2013.04.062