Abstract
BackgroundIn most species of aphid, female nymphs develop into either sexual or asexual adults depending on the length of the photoperiod to which their mothers were exposed. The progeny of these sexual and asexual females, in turn, develop in dramatically different ways. The fertilized oocytes of sexual females begin embryogenesis after being deposited on leaves (oviparous development) while the oocytes of asexual females complete embryogenesis within the mother (viviparous development). Compared with oviparous development, viviparous development involves a smaller transient oocyte surrounded by fewer somatic epithelial cells and a smaller early embryo that comprises fewer cells. To investigate whether patterning mechanisms differ between the earliest stages of the oviparous and viviparous modes of pea aphid development, we examined the expression of pea aphid orthologs of genes known to specify embryonic termini in other insects.ResultsHere we show that pea aphid oviparous ovaries express torso-like in somatic posterior follicle cells and activate ERK MAP kinase at the posterior of the oocyte. In addition to suggesting that some posterior features of the terminal system are evolutionarily conserved, our detection of activated ERK in the oocyte, rather than in the embryo, suggests that pea aphids may transduce the terminal signal using a mechanism distinct from the one used in Drosophila. In contrast with oviparous development, the pea aphid version of the terminal system does not appear to be used during viviparous development, since we did not detect expression of torso-like in the somatic epithelial cells that surround either the oocyte or the blastoderm embryo and we did not observe restricted activated ERK in the oocyte.ConclusionsWe suggest that while oviparous oocytes and embryos may specify posterior fate through an aphid terminal system, viviparous oocytes and embryos employ a different mechanism, perhaps one that does not rely on an interaction between the oocyte and surrounding somatic cells. Together, these observations provide a striking example of a difference in the fundamental events of early development that is both environmentally induced and encoded by the same genome.
Highlights
In most species of aphid, female nymphs develop into either sexual or asexual adults depending on the length of the photoperiod to which their mothers were exposed
Our results suggest that viviparous development in aphids does not use these components of the maternal terminal system, at least not in any way that resembles their use in Drosophila and Tribolium, raising questions about how asexual mothers are able to specify posterior fate in their daughter embryos
The pea aphid genome contains homologs of some, but not all, members of the Drosophila maternal terminal patterning system We searched for pea aphid homologs of members of the Drosophila maternal terminal system in the pea aphid genomic sequence [48], several of which had already been identified as the result of automated and manual annotation efforts [38] (Table 1)
Summary
In most species of aphid, female nymphs develop into either sexual or asexual adults depending on the length of the photoperiod to which their mothers were exposed. The progeny of these sexual and asexual females, in turn, develop in dramatically different ways. The fertilized oocytes of sexual females begin embryogenesis after being deposited on leaves (oviparous development) while the oocytes of asexual females complete embryogenesis within the mother (viviparous development). Viviparous ‘oocytes’ start out smaller and grow less than oviparous oocytes [5,6,7,8] In pea aphids, this means that viviparous oocytes range from one-third of the length of oviparous oocytes when first extruded to one-sixth just prior to vitellogenesis (Figure 1, compare arrows in C and D). Viviparous oocytes are surrounded by fewer somatic epithelial cells than oviparous oocytes (Figure 1, compare C and D)
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