The First Rejection

The first rejection: Eggs sequester bits of sperm for later elimination

May 4, 1998

Portions of the tail of gigantic fruit fly sperm, which enters the egg entirely during fertilization, persist in the developing midgut of the embryo and are excreted soon after the larva hatches, reports Tim Karr, a developmental biologist at the University of Chicago, and Scott Pitnick, an evolutionary biologist at the University of Syracuse in the May 7, 1998 issue of Proceedings of the Royal Society London B.

Karr and Pitnick, who have been studying the often bizarre sperm-egg interactions of Drosophila for several years, previously noticed that the long tails of fruit fly sperm entered the egg during fertilization, undermining the idea that the only role of the sperm tail is to propel its genetic cargo to the egg.

"It was remarkable that the egg accepted so much spermic material, especially since the tails of some sperm are over 20 times the length of the egg!" says Karr. "It became clear that the tail might be involved in the embryo's early development."

Now, using fluorescence staining, Karr and Pitnick have tracked the fate of the giant sperm tails of two species of fruit fly, D. melanogaster and D. pachea, throughout embryogenesis. They noticed that after the sperm entered the egg, its tail was partially degraded by the egg's enzymes, but otherwise remained intact and was sequestered in the developing embryo's midgut. One section of the tail was observed to remain untouched by the egg's enzymes. This particular segment could be seen in the guts of recently hatched larvae, where it appeared as a tight coil in photographs where the sperm had been stained with a fluorescent dye.

But when Karr and Pitnick looked for these pieces after the larvae were allowed to feed for a few hours, they were no longer detectable. Apparently, the larvae excrete the piece with their waste, says Karr, "We were pretty surprised that this segment persisted throughout the development of the embryo untouched."

Karr and Pitnick decided to look more closely at this stubborn section of sperm tail. Using electron microscopy, they determined that it was composed of what is called the mitochondrial derivative a crystallized form of the sperm's mitochondria. Mitochondria are normally inherited only from the mother, and provide energy for the cells. Because mitochondria have their own DNA, and replicate separately from the rest of the cell, they can pick up hazardous mutations just as the DNA of a cell's nucleus can. If mitochondria were inherited both maternally and paternally, the cell would have two genetically different sets of mitochondria, each of which could pick up mutations. By having only one genetic type of mitochondria inherited from the mother, the cell avoids the possibility of accumulating too many mutations in the mitochondria.

The fact that the entire sperm, including the mitochondrial derivative (which makes up about 50 percent of the tail) enters the egg means that a substantial amount of the father's mitochondrial DNA is present in the developing zygote. The researchers suspect that the egg sequesters the mitochondrial derivatives to the midgut as an active mechanism to avoid the inheritance of the father's mitochondrial DNA.

"Breaking down the derivative would require considerable amounts of energy," says Karr, "Sequestering it to the midgut where it will be eliminated is much easier." This mechanism works no matter how long the sperm's tail (and therefore the amount of mitochondrial derivative that can be packed into it) gets. The egg still rejects the paternal mitochondrial DNA by sequestering it to the developing fly's gut for future elimination.

This work indicates that "previously unrecognized sperm-egg interactions are important to the success of a developing zygote," says Karr. One intriguing possibility, he suggests, is that these interactions, which have been observed to be species-specific, may represent a reproductive barrier for inter-species hybrids, contributing significantly to reproductive isolation, one of the driving forces behind the origin of species.

Summary:
Portions of the tail of gigantic fruit fly sperm persist in the developing midgut of the embryo and are excreted soon after the larva hatches, reports Tim Karr, a developmental biologist at the University of Chicago, and colleagues in the May 7, 1998 issue of Proceedings of the Royal Society.