No abstract

Parthenogenesis has been documented in almost every phylum of animals, and yet this phenomenon is largely understudied. It has particular importance in dipterans since some parthenogenetic species are also disease vectors and agricultural pests. Here, we present a catalogue of parthenogenetic dipterans, although it is likely that many more remain to be identified, and we discuss how their developmental biology and interactions with diverse environments may be linked to different types of parthenogenetic reproduction. We discuss how the advances in genetics and genomics have identified chromosomal loci associated with parthenogenesis. In particular, a polygenic cause of facultative parthenogenesis has been uncovered in Drosophila mercatorum, allowing the corresponding genetic variants to be tested for their ability to promote parthenogenesis in another species, Drosophila melanogaster . This study probably identifies just one of many routes that could be followed in the evolution of parthenogenesis. We attempt to account for why the phenomenon has evolved so many times in the dipteran order and why facultative parthenogenesis appears particularly prevalent. We also discuss the significance of coarse genomic changes, including non-disjunction, aneuploidy, and polyploidy and how, together with changes to specific genes, these might relate to both facultative and obligate parthenogenesis in dipterans and other parthenogenetic animals.

From concatenated chromosomes to polyploidization, large-scale genome changes are known to occur in parthenogenetic animals. Here, we report mosaic aneuploidy in brains of facultatively parthenogenetic Drosophila. We identified a background of aneuploidy in D. mercatorum strains and found increased levels of aneuploidy in the brain tissue of animals arising parthenogenetically versus those arising from sexual reproduction. There is also variation in germline-derived aneuploidy between individuals within the strain. To determine if this is a general feature of facultative parthenogenesis in drosophilids, we compared sexually reproduced and parthenogenetic offspring from an engineered facultative parthenogenetic strain of D. melanogaster. In addition to germline-derived aneuploidy, this revealed somatic aneuploidy that increased by up to 4-fold in parthenogens compared to sexually reproduced offspring. Therefore, the genetic combination identified in D. mercatorum to cause facultative parthenogenesis in D. melanogaster results in aneuploidy, which indicates that the loss of mitotic control resulting in parthenogenesis causes subsequence genome variation within the parthenogenetic offspring. Our findings challenge the assumption that parthenogenetic offspring are near genetic replicas of their mothers.

Sexual reproduction evolved 1-2 billion years ago and underlies the biodiversity of our planet. Nevertheless, devolution of sexual into asexual reproduction can occur across all phyla of the animal kingdom. The genetic basis for how parthenogenesis can arise is completely unknown. To understand the mechanism and benefits of parthenogenesis, we have sequenced the genome of the facultative parthenogen, Drosophila mercatorum, and compared its organisation and expression pattern during parthenogenetic or sexual reproduction. We identified three genes, desat2, Myc, and polo in parthenogenetic D. mercatorum that when mis-regulated in a non-parthenogenetic species, D. melanogaster, enable facultative parthenogenetic reproduction. This simple genetic switch leads us to propose that sporadic facultative parthenogenesis could evolve as an 'escape route' preserving the genetic lineage in the face of sexual isolation.