Gene expression analysis of parthenogenetic embryonic development of the pea aphid, Acyrthosiphon pisum, suggests that aphid parthenogenesis evolved from meiotic oogenesis.

Aphids exhibit a form of phenotypic plasticity, called polyphenism, in which genetically identical females reproduce sexually during one part of the life cycle and asexually (via parthenogenesis) during the remainder of the life cycle. The molecular basis for aphid parthenogenesis is unknown. Cytological observations of aphid parthenogenesis suggest that asexual oogenesis evolved either through a modification of meiosis or from a mitotic process. As a test of these alternatives, we assessed the expression levels and expression patterns of canonical meiotic recombination and germline genes in the sexual and asexual ovaries of the pea aphid, Acyrthosiphon pisum. We observed expression of all meiosis genes in similar patterns in asexual and sexual ovaries, with the exception that some genes encoding Argonaute-family members were not expressed in sexual ovaries. In addition, we observed that asexual aphid tissues accumulated unspliced transcripts of Spo11, whereas sexual aphid tissues accumulated primarily spliced transcripts. In situ hybridization revealed Spo11 transcript in sexual germ cells and undetectable levels of Spo11 transcript in asexual germ cells. We also found that an obligately asexual strain of pea aphid produced little spliced Spo11 transcript. Together, these results suggest that parthenogenetic oogenesis evolved from a meiosis-like, and not a mitosis-like, process and that the aphid reproductive polyphenism may involve a modification of Spo11 gene activity.

Aphids: a model for polyphenism and epigenetics.

Environmental conditions can alter the form, function, and behavior of organisms over short and long timescales, and even over generations. Aphid females respond to specific environmental cues by transmitting signals that have the effect of altering the development of their offspring. These epigenetic phenomena have positioned aphids as a model for the study of phenotypic plasticity. The molecular basis for this epigenetic inheritance in aphids and how this type of inheritance system could have evolved are still unanswered questions. With the availability of the pea aphid genome sequence, new genomics technologies, and ongoing genomics projects in aphids, these questions can now be addressed. Here, we review epigenetic phenomena in aphids and recent progress toward elucidating the molecular basis of epigenetics in aphids. The discovery of a functional DNA methylation system, functional small RNA system, and expanded set of chromatin modifying genes provides a platform for analyzing these pathways in the context of aphid plasticity. With these tools and further research, aphids are an emerging model system for studying the molecular epigenetics of polyphenisms.