To adapt to hard winter conditions, many organisms living in temperate regions use photoperiod cues to anticipate the transition between autumn and winter. Such seasonal photoperiodism enables individuals to prepare winter installation through physiological or behavioural adaptations such as migration, hibernation or over-wintering egg-laying. Aphids are plant phloem feeding insects that provoke significant damage to agricultural crops. As poikiloterm animals, they do not regulate their internal temperature and die in cold winters. They bypass this difficulty by producing over-wintering eggs in the autumn that enter diapause during the winter period. Aphids are among the rare organisms practicing cyclical parthenogenesis during their annual life-cycle [1
], alternating between viviparous parthenogenesis and oviparous sexual reproduction. In spring, eggs hatch and the new born aphids develop clonal colonies by parthenogenesis: viviparous females produce other viviparous females that are genetically identical, without haploid gamete formation or meiotic recombination [2
]. At the end of the summer, these colonies produce, by clonal parthenogenesis, sexual morphs (males and oviparous females) that mate, these oviparous sexual females then lay eggs before winter.
In viviparous parthenogenetic aphids, embryos develop within the abdomen of their mother. Each mother contains several dozens of embryos at different stages of development. The most developed embryos have nearly complete differentiation of their ovaries with a germarium and several follicle chambers. Embryos at early stages are already formed within these follicle chambers. Thus, an adult viviparous female aphid contains two embedded generations: nearly fully developed embryos and early embryos within these developed embryos. This is the so-called "telescoping of generations".
The switch between parthenogenetic and sexual reproduction in aphids is driven by the variation of abiotic factors in autumn, primarily the photoperiod. Photoperiod shortening is sufficient to trigger the switch in the reproductive mode; decrease in temperature further promotes this switch [3
]. Aphids measure the length of the night phase (scotophase); a minimum number of consecutive inductive nights is required to trigger the switch in the reproductive mode [4
]. Several observations suggest that in aphids, part of the photoperiodic signal is detected by the protocerebrum in the brain through the cuticular head capsules [5
]. Several aphid putative photoreceptors and transducer proteins have been located in the protocerebrum and the compound eyes in Megoura viciae
]. Early transduction of the photoperiod signal involves a group of neurosecretory cells (Group I) located in the pars intercerebralis
of the aphid protocerebum [8
]. Transduction of the photoperiodic signal to the target tissues and cells located in the ovaries is still unresolved; however, ectopic applications of melatonin [9
] or juvenile hormones [10
] suggest that these molecules play key roles in the oocyte fate. During viviparous parthenogenesis, the photoperiodic signal may be detected and/or transduced through the different embedded generations; the regulatory mechanisms of such trans-generational signalling are not known.
Recently, with the development of genomic tools for the pea aphid Acyrthosiphon pisum
], global analyses of gene regulation have been undertaken between aphids producing or not sexual. A receptor of GABA whose mRNA is up-regulated in long-night reared insects has already been identified [14
]. Our group was the first to demonstrate that genes encoding cuticle and signalling proteins are regulated by shortening of the photoperiod [15
]. To date, these studies have been performed on one development stage and during only one generation.
Herein, we analysed the transcriptomic and proteomic response of the pea aphid to shortening of the photoperiod at different stages covering the two parthenogenetic generations required before the birth of the future sexuals. We observed very few transcripts were regulated in the heads of the grand-mothers. In contrast, major changes occurred in the heads of mothers of the future sexual; these are probably linked to the developmental program of parthenogenetics that are sexual producers. Genes with putative functions in visual cues, photoreception, cuticle structure and the insulin pathway are particularly discussed.