Background. Socially transferred materials (STMs), such as sperm, eggs, seminal fluid and milk, are made or processed in one individual’s body and transferred to another, where they act on the recipient’s physiology. STMs are central to reproduction in a variety of ways and are often essential. Broadly, long conserved genes tend to be important for function. Here, combining proteomics of STMs and ancestral state reconstruction allow us to determine the deep-time evolution of socially transferred protein compartments.
Methods. We built a phyloproteomic framework that pairs comparative proteomics of a transferred material across many species with phylogenomics across 71 eukaryotes, decoupling three usually conflated events: a gene family’s genomic birth, its expansion, and its recruitment into the material. We applied it first to sperm, using proteomes from 32 animal species, and are extending it to eggs and milk-like substances across animals.
Results. For sperm, we define a conserved core of 304 gene families present in the sperm of the metazoan ancestor. We find 80% were already deployed at the last eukaryotic common ancestor, 11% in choanoflagellates, and only 9% is animal-specific, making animal sperm a co-opted unicellular legacy rather than a multicellular invention. Evolutionary age maps onto subcellular architecture, with ancient components building the flagellum and younger ones the fertilisation interface. The oldest components are disproportionately linked to monogenic male infertility in humans, mice and Drosophila, while conserved animal-specific components emerge as candidates for non-hormonal contraception.
Conclusion. Phyloproteomics turns a socially transferred material into a set of datable objects, separating ancient, constrained components from recent, labile ones and flagging those of potential clinical importance. Extended across sperm, egg and milk, this offers reproductive biology a general, evolution-guided way to prioritise molecules and models for fertility and contraception.