Pervasive convergent evolution of sperm conjugation across the Arthropoda tree of life

Theory suggests that ejaculates should evolve heightened functionality
through integration of their component parts: spermatozoa, seminal fluid,
and ejaculate structures. Here, we exhaustively review the vast literature
on sperm ultrastructure in arthropods to examine sperm conjugation - a
form of social cooperation among sperm - in addition to its relationship
with an ostensible antecedent: membrane-bound, extracellular
sperm-associated material (SAM). Our reconstructions suggest that sperm
conjugation first arose on the branch leading to insects and remipedes
during the Cambrian or Ordovician Periods (i.e., 452.6 – 508.5 million
years ago). Since then, arthropods and related ecdysozoans have spent an
estimated two-thirds of their time with sperm conjugation, which has been
evolutionarily lost and gained approximately 45 times each. We show that
most evolutionary derivations of conjugation occurred following the origin
of SAM, with SAM in "proto-conjugates" facilitating subsequent
diversification of multiple conjugate types. Finally, comparative analyses
of proteomes of the convergently-derived spermatostyles (specialized rods
of SAM to which sperm attach) of true bugs and beetles indicate parallel
utilization of a common genetic toolkit that may draw upon deep homology
for the evolution of complex ejaculate adaptations. Our analyses reveal an
ancient, pervasive and dynamic history of evolutionary experimentation
with ejaculate form and function.