The Mitochondrial bottleneck: strict sex-specific mtDNA segregation in the germline of the DUI species Veneripis philippinarum (Bivalvia Veneridae)

Doubly Uniparental Inheritance (DUI) is one of the most striking exceptions to the common rule of Strict Maternal Inheritance (SMI) of metazoan mitochondria and has been found in several bivalve species. In DUI, two mitochondrial genomes are present, showing different transmission routes, one through eggs (F-Type), the other through sperm (M-Type). Moreover, M- and F-Types experience peculiar tissue distributions, with males being heteroplasmic in their soma, while females usually not. We performed a Real-Time Multiplex qPCR analysis on the Manila clam Venerupis philippinarum to quantify M- and F-Types in somatic tissues, gonads and gametes, as well as mtDNA duplication rates during early embryo development. In most male somatic tissues, the MType is largely predominant; something similar is found for a few females too, actually showing MmtDNAs in their soma. On the contrary, in the germline we evidenced a strict sex-specific mtDNA segregation, since both sperm and eggs do carry exclusively M- and F-Type respectively. Because of this, we propose that the sex-specific mtDNA transmission is achieved through a 3-checkpoint process. The cytological mechanisms of male mitochondria segregation in males and degradation in females during the early embryo development (that we named checkpoints #1 and #2) are already known for DUI species; we propose for the first time, a third checkpoint that would act when Primordial Germ Cells (PGCs) are first formed and would work for both mtDNAs. DUI provides a privileged point of view to unveil the processes by which mitochondria enter the germline (i.e. the “mitochondrial bottleneck”) and the evidences we observed on a strict selection of sex-specific mtDNAs in the germline could be a first step in that direction. Actually, a sound working hypothesis is that these processes might be based on similar molecular mechanisms in SMI species.