Extended Data Fig. 8: From sexual parasitisms to xenoparous reproduction.

Species that act as sexual parasites use another species’s gametes to propagate their own genome³. Such sexual parasitism can be divided into two main categories illustrated at the top of this figure (a and b). Xenoparous reproduction (this study) is illustrated at the bottom of the figure (c). a, Sperm parasitism. A female exploits the sperm of another species to reproduce. The most typical form of sperm parasitism is gynogenesis, where females reproduce asexually but require contact with sperm to initiate embryogenesis. After contact, the host male’s genome is immediately excluded⁸⁸. In contrast, this exclusion is delayed to the next generation in hybridogenesis. In this alternate form of sperm parasitism, the male genome is present in the somatic cells of the parasite offspring but excluded during meiosis when germinal cells are produced⁸⁹. In social insects, hybridogenesis refers to cases where the male genome is present in workers (i.e. somatic cells of a “superorganism”) but excluded from reproductive individuals (i.e. germinal cells of a “superorganism”). Such social hybridogenesis is common in the Messor genus¹² and is the sperm parasitism at the origin of xenoparous reproduction in Messor ibericus (see Fig. 3a). b, Ova parasitism. A male exploits the ova of another species to reproduce. Typically referred as male cloning, androgenesis is the flip side of gynogenesis, where offspring only carry the nuclear genome of their father. It is excessively rare compared with gynogenesis and typically occurs in a hermaphrodite context with exceptional inter-specific parasitism (Cupressus dupreziana conifers or Corbicula clams)^25,26,27. To date, male clonality is restricted to intraspecific cases in ants^29,30,31. c, Xenoparous reproduction. Here, females need to produce males of the other species, as both species rely on each other’s gametes. This combines elements of both sexual parasitism forms, but with a key difference: females are not victims of ova parasitism but require it, as it is the case for males regarding sperm parasitism. In the sole case known so far (this study) sp1 females “use” sp2 male sperm for worker production, while sp2 males “use” sp1 female ova for cloning. Since sp1 females and sp2 males share the same colonies, both species benefit from having their gametes exploited by the other, as both require workers and males. By integrating sperm and ova parasitism into a single superorganism, such a “sexual domestication” neutralizes the sex war, as both species are trapped into a self-sufficient unit of selection. As it results in a cohesive reproductive unit of two species, evolution toward xenoparity can be qualified as an evolutionary transition in individuality^49,50.