Independent origin of sperm heteromorphism in the Drosophilidae

Sperm heteromorphism, the production multiple discrete sperm types (or
"morphs"), occurs in diverse animal and plant taxa. This
phenomenon represents a division of labor by male gametes, with one morph
participating in fertilization and the other morph(s) specialized to
perform some other reproductive function. One of the most intensively
investigated systems is the Drosophila obscura species group, for which
sperm heteromorphism evolved once in the common ancestor to the group,
with all examined descendent species exhibiting sperm length
heteromorphism. The absence of additional sperm heteromorphism origins
among drosophilids has precluded comparative evolutionary analyses. Here,
we report the discovery of a second origin within the Drosophilidae, with
Chymomyza procnemis exhibiting the most extreme sperm length
heteromorphism known (> 15-fold difference). Males produced and
transferred to females approximately twice as many short sperm as long
sperm. Shortly after insemination, females ejected from their reproductive
tracts most of the short morph sperm, yet relatively few of the long morph
sperm, resulting in a preponderance of long morph sperm occupying the
females' sperm-storage organs. By the start of egg laying, few-to-no
short morph sperm were detectable in females. Although C. procnemis have
very long eusperm and the highest relative investment (Gonadosomatic
Index; GSI) in testes for any drosophilid species, a comparative analysis
of 149 Drosophila species revealed no significant coevolutionary
relationship between sperm heteromorphism and either sperm length or GSI.
Continued investigations with Chymomyza will advance our understanding of
how sperm heteromorphism arises, persists, and diversifies across
lineages.