The extraembryonic serosa protects the insect egg against desiccation

Proc Biol Sci. 2013 Jun 19;280(1764):20131082. doi: 10.1098/rspb.2013.1082. Print 2013 Aug 7.

Abstract

Insects have been extraordinarily successful in occupying terrestrial habitats, in contrast to their mostly aquatic sister group, the crustaceans. This success is typically attributed to adult traits such as flight, whereas little attention has been paid to adaptation of the egg. An evolutionary novelty of insect eggs is the serosa, an extraembryonic membrane that enfolds the embryo and secretes a cuticle. To experimentally test the protective function of the serosa, we exploit an exceptional possibility to eliminate this membrane by zerknüllt1 RNAi in the beetle Tribolium castaneum. We analyse hatching rates of eggs under a range of humidities and find dramatically decreasing hatching rates with decreasing humidities for serosa-less eggs, but not for control eggs. Furthermore, we show serosal expression of Tc-chitin-synthase1 and demonstrate that its knock-down leads to absence of the serosal cuticle and a reduction in hatching rates at low humidities. These developmental genetic techniques in combination with ecological testing provide experimental evidence for a crucial role of the serosa in desiccation resistance. We propose that the origin of this extraembryonic membrane facilitated the spectacular radiation of insects on land, as did the origin of the amniote egg in the terrestrial invasion of vertebrates.

Keywords: Tribolium castaneum; chs (chitin synthase); cuticle; desiccation resistance; zen (zerknüllt).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biological Evolution
  • Chitin Synthase / genetics
  • Dehydration
  • Embryo, Nonmammalian / anatomy & histology*
  • Embryo, Nonmammalian / cytology
  • Gene Expression Regulation, Developmental
  • Insect Proteins / genetics
  • Insecta / embryology
  • Ovum / cytology
  • RNA Interference
  • Serous Membrane / embryology*
  • Tribolium / embryology*
  • Tribolium / genetics

Substances

  • Insect Proteins
  • Chitin Synthase