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At Cornell, Dawn Chen was counting sperm stored in a pair of organs called spermathecae in female fruit flies, fully expecting the counts to be roughly the same. The two spermathecae, which store and release sperm after a female mates, look identical, so Chen was surprised to find significantly different sperm counts between the two.

The result kicked off an investigation involving four labs from three different universities that provides an example of the evolutionary and developmental basis for asymmetry, a pattern found throughout biology where a pair of organs or appendages that mirror each other have different proportions and may have different functions. Examples include fiddler crab claws, or bird ovaries, as birds have two but most use only one.

The findings, reported in a published in the Proceedings of the National Academy of Sciences, open new avenues for understanding how asymmetries arise and may impact reproductive success.

The study is a collaboration among labs from Cornell, New York University and the Hebrew University of Jerusalem, which each brought unique expertise to the research to arrive at their overall conclusions.

The paper reveals that spermathecae in female fruit flies appear symmetrical but actually function in significantly different ways and each originate from different lineages.

These asymmetries are likely maintained in species because members of a pair specialize in ways that are likely to create evolutionary advantages, according to the paper.

"In this particular case, mutations arise and sometimes they can have these asymmetric effects, but it's essentially straight-up evolution—it's favorable somehow or another," said Andrew Clark, the Jacob Gould Schurman Professor of Population Genetics and Nancy and Peter Meinig Family Investigator in the College of Arts and Sciences and a senior co-author of the paper. "The idea that these two spermathecae might be able to confer some advantage if they have different functions is almost inevitable," he said.

At Cornell, Mariana Wolfner, Distinguished Professor of Molecular Biology and Genetics and a Stephen H. Weiss Presidential Fellow in the College of Arts and Sciences, was also a senior co-author of the paper.

When Chen, a former doctoral student of both Wolfner's and Clark's and the paper's first author, happened upon the discovery, they were studying the process of sperm preference or competition, such as whose sperm has a greater chance to fertilize eggs when two or more fruit fly (Drosophila melanogaster) males mate with a female. Female fruit flies are known to mate as often as once a day, with different males.

Chen, due to a meticulous nature, counted and recorded sperm separately for the two spermathecae, and that was when they found that each spermatheca stored and released sperm at different rates.

"When the group did the statistics, it was clear the spermathecae in a pair stored different amounts of sperm and had a different release rate, which was shocking to us at the time," Wolfner said.

In D. melanogaster and in many other species, there has been a long-standing question of whether males can displace sperm from previous males within the female, and in that way control parentage, or whether females can control sperm release rates from spermathecae, part of a larger process called post-copulatory sexual selection.

"If the female can control whose sperm fertilizes an egg, for example by controlling sperm-release rates, it's one way that she can seize control over which male 'wins' to have progeny with her," Wolfner said.

Meanwhile, senior co-author Mark Siegal, a professor of developmental evolutionary biology at New York University, had been investigating how spermathecae developed.

"Everyone expected that the two spermathecae developed the same way," Wolfner said. Siegal used a special genetic technique, called G-TRACE, that allowed him to mark the descendants of a particular cell.

"And when he did that, he discovered that the two spermathecae each derived from a different cell-lineage, which was shocking because they look identical," Wolfner said.

One spermatheca originated from progenitor cells that expressed a gene called wingless; the other from progenitor cells that expressed a gene called engrailed. These two genes influence a wide range of biological processes in animals from insects to humans.

Chen then used the G-TRACE technique to distinguish between the two spermathecae and counted the sperm in each, finding that the spermathecae differed in sperm-release rates depending on which lineage they came from.

In addition, senior co-author Yael Heifetz, an expert on the female D. melanogaster reproductive tract at the Hebrew University of Jerusalem, uncovered differences in size and secretory activity between the two spermathecae.

Co-authors include doctoral student Jonathon Thomalla in Wolfner's lab and postdoctoral researcher Yassi Hafezi in Clark's lab.