Paternal products and by–products in Drosophila development

Abstract

Tails of fertilizing spermatozoa persist throughout embryogenesis in Drosophila species and can be observed within the midguts of larvae after hatching. Throughout development, sperm proteins slowly di¡use or are stripped from the giant sperm tail residing within the embryo's anterior end. The shape and position of the sperm within the embryo are regulated such that, during organ formation, the unused portion of the sperm is enveloped by the developing midgut. This persistent, paternally derived structure is composed of the sperm's mitochondrial derivatives and appears to be defaecated by the larva soon after hatching. These complex sperm^egg interactions may represent mechanisms to avoid intragenomic con£ict by ensuring strictly maternal inheritance of mitochondrial DNA (mtDNA).

Paternal transmission of mitochondrial DNA as an integral part of mitochondrial inheritance in metapopulations of Drosophila simulans

“…We deem temperature unlikely a major driving force in our study because temperature was kept constant in our experiments and a temperaturedependent effect, if occurring, should have been observable in both mating directions. An uneven distribution of mtDNA haplotypes could also be caused by a bottleneck effect or by random assortment of large mitochondrial sperm derivates (assuming these contain mtDNA) during early developmental stages (Bergstrom and Pritchard, 1998;Pitnick and Karr, 1998). These are stochastic processes, however, and are thus not in agreement with the observed pair-specific distribution of paternal leakage here.…”

“…First, the directed sequestration of mitochondrial sperm derivatives into the midgut and subsequent defecation during early embryonic development, a mechanism put forward to exclude paternal mtDNA from inheritance in D. melanogaster and D. pachea (Pitnick and Karr, 1998). A failure of this mechanism could potentially lead to the inclusion of paternal mtDNA within the developing embryo.…”

“…Contrary to the long prevailing, but finally discredited hypothesis that paternal mtDNA is excluded from the animal zygote by the exclusion of the sperm tail containing the mitochondria, we now know that it is rather the interplay of several stochastic and molecular mechanisms that inhibits the transmission of paternal mtDNA (Pitnick and Karr, 1998;White et al, 2008;DeLuca and O'Farrell, 2012). These mechanisms include: (i) the dilution of paternal by maternal mtDNA in the zygote, that is, paternal mtDNA is vastly outnumbered by maternal mtDNA, (ii) the selective tagging (ubiquitination) and subsequent destruction of paternal sperm mitochondria upon fertilization in mammals (Sutovsky et al, 1999(Sutovsky et al, , 2000 and (iii) the presence of a genetic bottleneck during early developmental stages that is likely to exclude minor allele contributions, for example, paternal mtDNA (Bergstrom and Pritchard, 1998;White et al, 2008).…”

Gametic incompatibilities between races ofDrosophila melanogaster

“…There is ample evidence that the reproductive tract is among the most rapidly evolving of all phenotypic traits (Eberhard 1985(Eberhard , 1996Thomas & Singh 1992;Rice & Holland 1997;Hellriegel & Ward 1998;Pitnick & Karr 1998). Rice (1996), Rice & Holland (1997) and Holland & Rice (1999) showed that, when female evolution is experimentally halted, males actually become toxic to females.…”

Giant sperm in a Neotropical moth Xenosoma geometrina (Lepidoptera: Arctiidae)

“…Theory predicts that any advantages in producing such large sperm have little to do with providing resources to the devel oping zygote (Parker, 1982). Indeed Pitnick & Karr (1998) have found that the tails of fertilizing sperm persist throughout embryogenesis in Drosophila species and are sequestered within the midguts of the developing larvae. They are later defecated by the larvae after hatching.…”