Gene Expression Analysis of Parthenogenetic Embryonic Development of the Pea Aphid, Acyrthosiphon pisum, Suggests That Aphid Parthenogenesis Evolved from Meiotic Oogenesis

Abstract

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.

Direct flow cytometry measurements reveal a fine-tuning of symbiotic cell dynamics according to the host developmental needs in aphid symbiosis

“…The absolute number of B. aphidicola cells appeared to increase with maternal development. In fact, as the parthenogenetic viviparous females grow, the embryonic chains gradually develop and they consist of more and more mature embryos 14 42 43 , which are, in turn, expected to contain an increasing number of symbiotic bacteria (i.e. endosymbionts, initially transferred in early embryos after blastoderm cellularization, are suspected of undergoing numerous division cycles during embryo maturation).…”

Chromosome Unipolar Division and Low Expression of Tws May Cause Parthenogenesis of Rice Water Weevil (Lissorhoptrus oryzophilus Kuschel)

“…In ploidy restoration of parthenogenetic animals, meiosis is either preserved in some form (automixis) or is largely suppressed (parthenogenesis) [ 14 ]. Obligate parthenogenesis RWW is a triploid organism, which is different from silkworms ( Bombyx mori ) and aphids ( Acyrthosiphum pisum ) [ 24 , 47 , 48 , 49 , 50 , 51 , 52 , 53 , 54 ] [ 55 ] (pp. 199–257) whose reproductive strategies can be changed by environmental factors.…”

“…Moreover, parthenogenetic RWW does not require sperm to participate in the entire life cycle, which is different from nematodes ( Mesorhabditis belari ) [ 56 ] that require sperm to activate unfertilized eggs for parthenogenesis. These results imply that diploid parthenogenetic organisms retain the complete meiotic process and meiotic genes [ 20 , 53 ]. In triploid parthenogenetic male Cacopsylla myrtilli meiosis, all univalent chromosomes divide during the first meiotic division resulting in the incomplete second meiotic division and formation of diploid sperms [ 57 , 58 , 59 ].…”

Antifeedant activity of long-chain alcohols, and fungal and plant metabolites against pea aphid (Acyrthosiphon pisum) as potential biocontrol strategy

“…The widespread and systematic use of chemicals and the use of biocontrol strategies does not provide the required control due to the complex PA life cycle (Blackman and Eastop 2014) and their easy environmental adaptation (Tares et al 2013;Srinivasan et al 2014) and risk of development of resistance to pesticides (Vanlerberghe-Massutti and Guillemaud 2007). Nowadays the overuse of chemicals as insecticides is being questioned, regarding the massive environmental damage, their human and animal health risks and application costs (Coats 1994;Schraeder et al 2010).…”