Molecular anatomy of an onychophoran: compartmentalized sperm storage and heterogeneous paternity

Onychophorans (peripatus or velvet worms) show extraordinarily high local endemism, and cryptic species are common. As part of a programme addressing issues of endemicity at hierarchical spatial scales, we investigated reproduction in Euperipatoides rowelli (Onychophora: Peripatopsidae) using microsatellite analysis. This species is ovoviviparous, and females have up to 70 embryos in their uteri simultaneously. Batches of undeveloped and well-developed embryos may be present in the uteri of a female. Paired ovaries lead via a common oviduct into paired uteri, each of which has a spermatheca (sperm storage organ). Insemination in E. rowelli is dermal-haemocoelic: spermatophores are placed on the skin of the female, the body wall is breeched, and sperm are released into the haemocoel through which they migrate to the spermathecae. There is no obvious mechanism to prevent sperm mixing, yet microsatellite analysis indicated that offspring in a female's paired reproductive tracts can be sired by different males, and that the paired spermathecae can contain sperm from different males. More than 70% of females had broods with multiple paternity. The data are consistent with the potential for female postcopulatory influence over fertilizations: in particular, compartmentalization of sperm from different males into different spermathecae. Female control of fertilizations could lead to benefits including increased diversity of offspring, minimization of maternal-paternal genetic incompatibility, and influence on offspring genotypes. Multiple mating alone may increase the genetic diversity of offspring: this could be of importance in E. rowelli, which has very small genetic neighbourhoods and low genetic marker diversity.