A comparison of parthenogenetic and sexual embryogenesis of the pea aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea)

Abstract

Aphids exhibit divergent modes of embryogenesis during the sexual and asexual phases of the life cycle. To explore how a single genome can give rise to these alternative developmental modes, we have initiated embryological studies of the pea aphid, Acyrthosiphon pisum. Here we present a detailed description of parthenogenetic, viviparous embryonic development in the pea aphid. We compare and contrast development of the parthenogenetic embryo with that of the embryo resulting from sexual reproduction. The primary difference between the embryos is the scale on which development occurs: early parthenogenetic development occurs in a volume approximately three orders of magnitude smaller than the sexual egg, largely because of the apparent absence of yolk in the parthenogenetic egg. This results in a drastically different duration of syncytial energid cleavage and, presumably, patterning processes in the two embryos must act at scales that differ by orders of magnitude. The eggs also develop on time scales that differ approximately by an order of magnitude and the timing of the embryonic movements, collectively called blastokinesis, have temporally shifted relative to growth of the embryo. In addition, the endosymbiotic bacteria are transferred from mother to embryo in different ways in the two embryos. Finally, the function of the serosa has diverged greatly in the two embryos: in the sexual egg the serosa deposits a thick cuticle that protects the egg, whereas the serosa of the parthenogenetic embryo is greatly reduced and its function is unclear. The pea aphid is a useful model system for examining how a single genome has evolved to allow divergent modes of development.

Signatures of host/symbiont genome coevolution in insect nutritional endosymbioses

“…The ease of maintaining a continuous supply of asexual embryos vs. the difficulty of maintaining a steady supply of sexually produced embryos means that most recent work has focused on Buchnera transmission during asexual reproduction (53). That said, during both sexual and asexual reproduction in A. pisum it is clear that Buchnera do not localize to the germarium at any point in development and that each developing oocyte (in the case of sexual reproduction) or embryo (in the case of asexual reproduction) receive Buchnera from a single maternal bacteriocyte cell (13,(53)(54)(55). The most recent model of endosymbiont transmission, which was built from examination of transmission electron micrograph images of Buchnera transmission in asexual A. pisum, demonstrates that Buchnera transmission occurs by a process of exo/endocytosis (53).…”

Transgenerational seasonal timer for suppression of sexual morph production in the pea aphid, Acyrthosiphon pisum

“…These females laid eggs on the leaf or on the ceiling of the case after approximately 10 days. These eggs were used for experiments, except for those that did not darken within a few days and were judged as unfertilized (Miura et al, 2003). Fertilized eggs were kept under SD at 15.0 ± 1.0°C for seven days, and then placed under constant darkness at 4.0 ± 1.0°C for approximately three months to ensure embryogenesis Via, 1992).…”

An ancient but promiscuous host–symbiont association between Burkholderia gut symbionts and their heteropteran hosts

“…In general, such microbial partners are maintained through host generations by specialized transmission mechanisms (Buchner, 1965;Bourtzis and Miller, 2003;Kikuchi, 2009;Bright and Bulgheresi, 2010). For example, an intracellular symbiont Buchnera in aphids is providing essential amino acids for the host, indispensable for the host growth and reproduction, and transovarially transmitted to eggs or embryos in the maternal host body (Douglas, 1998;Miura et al, 2003). Meanwhile, insects harboring extracellular gut symbionts of mutualistic nature, like termites and stinkbugs, have evolved posthatch mechanisms for symbiont transmission, such as superficial microbial contamination of eggs (egg smearing) and probing of parental microbecontaining excrement (coprophagy) (reviewed in Buchner, 1965).…”