The transcriptome of Icerya aegyptiaca (Hemiptera: Monophlebidae) and comparison with neococcoids reveal genetic clues of evolution in the scale insects

Abstract

Background Scale insects are worldwide sap-sucking parasites, which can be distinguished into neococcoids and non-neococcoids. Neococcoids are monophyletic with a peculiar reproductive system, paternal genome elimination (PGE). Different with neococcoids, Iceryini, a tribe in non-neococcoids including several damaging pests, has abdominal spiracles, compound eyes in males, relatively abundant wax, unique hermaphrodite system, and specific symbionts. However, the current studies on the gene resources and genomic mechanism of scale insects are mainly limited in the neococcoids, and lacked of comparison in an evolution frame. Result We sequenced and de novo assembled a transcriptome of Icerya aegyptiaca (Douglas), a worldwide pest of Iceryini, and used it as representative of non-neococcoids to compare with the genomes or transcriptomes of other six species from different families of neococcoids. We found that the genes under positive selection or negative selection intensification (simplified as “selected genes” below) in I. aegyptiaca included those related to neurogenesis and development, especially eye development. Some genes related to fatty acid biosynthesis were unique in its transcriptome with relatively high expression and not detected in neococcoids. These results may indicate a potential link to the unique structures and abundant wax of I. aegyptiaca compared with neococcoids. Meanwhile, genes related to DNA repair, mitosis, spindle, cytokinesis and oogenesis, were included in the selected genes in I. aegyptiaca, which is possibly associated with cell division and germ cell formation of the hermaphrodite system. Chromatin-related process were enriched from selected genes in neococcoids, along with some mitosis-related genes also detected, which may be related to their unique PGE system. Moreover, in neococcoid species, male-biased genes tend to undergo negative selection relaxation under the PGE system. We also found that the candidate horizontally transferred genes (HTGs) in the scale insects mainly derived from bacteria and fungi. bioD and bioB, the two biotin-synthesizing HTGs were exclusively found in the scale insects and neococcoids, respectively, which possibly show potential demand changes in the symbiotic relationships. Conclusion Our study reports the first I. aegyptiaca transcriptome and provides preliminary insights for the genetic change of structures, reproductive systems and symbiont relationships at an evolutionary aspect. This will provide a basis for further research and control of scale insects.