Evolution, Development, and the Incoherence of Sex: A Framework for Multiple Sex Concepts

The word sex can refer to at least seven distinct, evolutionarily related biological phenomena (0-6 below). Bacteria and archaea use mechanisms for horizontal gene transfer (0) broadly and promiscuously, even without cell contact. Their endosymbiotic merger led to eukaryotes and a new form of gene exchange, using syngamy and meiosis (1) to mix and recombine similar genomes. This innovation altered the course of evolution. The requirement for chromosome homology in meiosis separated evolving lineages. Mating types evolved within them, differentiating roles of the cells pairing in syngamy, and gamete size dimorphisms (2) evolved many times. Organisms evolved diverse gamete-production strategies (3) and a plethora of traits associated with those strategies (4). They also evolved many ways to facilitate gamete encounters (5). Some of these were expressed in other contexts and gained new functions (6). These phenomena include cellular genetic processes (0 and 1), alternative states of cells and organisms (2-4), and things organisms do (5 and 6) that have diversified over billions of years. Sex is neither biologically simple nor conceptually singular, but the word is often used without qualifiers, assuming shared understanding that may not exist. We present a framework for multiple sex concepts that serve as anchor points to discuss the relationships among these phenomena and the diversity and complexity of each, including the biologically fuzzy edges generated by developmental variation and evolutionary change. We highlight several communication challenges that may limit biological understanding and/or facilitate the deployment of biology to justify social harms. For instance, sex is used for three alternative-state concepts (2-4 above) whose distinctions are sometimes collapsed, fostering overgeneralization based on the supposed simplicity of anisogamy, but even gamete sex is evolutionarily complex and subject to shifting definitional criteria. Attempts to narrowly bound "biological sex" minimize this complexity and what we can learn from it, while facilitating the misuse of biology in antidiversity social projects. Another challenge is that using accessible language that works for organisms like ourselves may misrepresent or obscure the biology of other life forms, but specialized language can create information silos; these limit the broad comparisons that are necessary both for perspective on our own biology and a more expansive understanding of life. The multiple sex concepts framework is a way to acknowledge the scope and discuss the complexity of sex in biology, offering a scaffold to facilitate broader thinking, better communication, and discovery.