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.
References
- 1
Grimaldi DA& Engel MS . 2005 Evolution of the insects. New York, NY: Cambridge University Press. Google Scholar - 2
Zeh DW, Zeh JA& Smith RL . 1989 Ovipositors, Amnions and eggshell architecture in the diversification of terrestrial arthropods. Q. Rev. Biol. 64, 147–168.doi:10.1086/416238 (doi:10.1086/416238). Crossref, ISI, Google Scholar - 3
- 4
Beament JWL . 1951 The structure and formation of the egg of the fruit tree red spider mite, Metatetranychus ulmi Koch. Ann. Appl. Biol. 38, 1–24.doi:10.1111/j.1744-7348.1951.tb07787.x (doi:10.1111/j.1744-7348.1951.tb07787.x). Crossref, ISI, Google Scholar - 5
Foelix RF . 1996 Biology of spiders, 2nd edn, p. 330. Oxford, UK: Oxford University Press. Google Scholar - 6
- 7
Lees AD . 1948 Passive and active water exchange through the cuticle of ticks. Discuss. Faraday Soc. 3, 187–192.doi:10.1039/df9480300187 (doi:10.1039/df9480300187). Crossref, Google Scholar - 8
Witaliñski W . 1993 Egg shells in mites: vitelline envelope and chorion in Acaridida (Acari). Exp. Appl. Acarol. 17, 321–344.doi:10.1007/bf00058596 (doi:10.1007/bf00058596). Crossref, ISI, Google Scholar - 9
Norris KR . 1950 The aestivating eggs of the Red-legged earth mite, Halotydeus destructor (Tucker). Bull. Commonw. Sci. Indust. Res. Aust. 253, 1–26. Google Scholar - 10
Giribet G& Edgecombe GD . 2012 Re-evaluating the arthropod tree of life. Annu. Rev. Entomol. 57, 167–186.doi:10.1146/annurev-ento-120710-100659 (doi:10.1146/annurev-ento-120710-100659). Crossref, PubMed, ISI, Google Scholar - 11
Regier JC, Shultz JW, Zwick A, Hussey A, Ball B, Wetzer R, Martin JW& Cunningham CW . 2010 Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature 463, 1079–1083. See http://www.nature.com/nature/journal/v463/n7284/suppinfo/nature08742_S1.html. Crossref, PubMed, ISI, Google Scholar - 12
Jura C . 1972 Development of apterygote insects. Developmental systems: insects (eds, Counce SJ& Waddington CH ), pp. 49–94. London, UK: Academic Press Inc. Google Scholar - 13
Machida R . 2006 Evidence from embryology for reconstructing the relationships of hexapod basal clades. Arthropod Syst. Phylogeny 64, 95–104. Google Scholar - 14
Machida R& Ando H . 1998 Evolutionary changes in developmental potentials of the embryo proper and embryonic membranes along with the derivative structures in atelocerata, with special reference to hexapoda (Arthropoda). Proc. Arthropod Embryol. Soc. Jpn 33, 1–13. Google Scholar - 15
Anderson DT . 1973 Embryology and phylogeny in annelids and arthropods. Oxford, UK: Pergamon Press. Google Scholar - 16
Dearden PK, Donly C& Grbić M . 2002 Expression of pair-rule gene homologues in a chelicerate: early patterning of the two-spotted spider mite Tetranychus urticae. Development 129, 5461–5472.doi:10.1242/dev.00099 (doi:10.1242/dev.00099). Crossref, PubMed, ISI, Google Scholar - 17
Mittmann B& Wolff C . 2012 Embryonic development and staging of the cobweb spider Parasteatoda tepidariorum C. L. Koch, 1841 (syn.: Achaearanea tepidariorum; Araneomorphae; Theridiidae). Dev. Genes Evol. 222, 189–216.doi:10.1007/s00427-012-0401-0 (doi:10.1007/s00427-012-0401-0). Crossref, PubMed, ISI, Google Scholar - 18
Wolff C& Hilbrant M . 2011 The embryonic development of the central American wandering spider Cupiennius salei. Front. Zool. 8, 1–35.doi:10.1186/1742-9994-8-15 (doi:10.1186/1742-9994-8-15). Crossref, PubMed, ISI, Google Scholar - 19
Korschelt E& Heider K . 1936 Vergleichende Entwicklungsgeschichte der Tiere. New York, NY: Fischer. Google Scholar - 20
Laurie M . 1890 The embryology of a scorpion (Euscorpius italicus). Q. J. Microsc. Sci. 31, 105–142. Google Scholar - 21
Rafiqi AM . 2008 Morphological transitions and the genetic basis of the evolution of extraembryonic tissues in flies. PhD thesis, Wageningen University, Wageningen, The Netherlands. Google Scholar - 22
Larink O& Bilinski SM . 1989 Fine structure of the egg envelopes of one proturan and two Collembolan genera (Apterygota). Int. J. Insect Morphol. Embryol. 18, 39–45.doi:10.1016/0020-7322(89)90034-2 (doi:10.1016/0020-7322(89)90034-2). Crossref, Google Scholar - 23
Brena C& Akam M . 2012 The embryonic development of the centipede Strigamia maritima. Dev. Biol. 363, 290–307.doi:10.1016/j.ydbio.2011.11.006 (doi:10.1016/j.ydbio.2011.11.006). Crossref, PubMed, ISI, Google Scholar - 24
Browne WE, Price AL, Gerberding M& Patel NH . 2005 Stages of embryonic development in the amphipod crustacean, Parhyale hawaiensis. Genesis 42, 124–149.doi:10.1002/gene.20145 (doi:10.1002/gene.20145). Crossref, PubMed, ISI, Google Scholar - 25
Extavour CG . 2005 The fate of isolated blastomeres with respect to germ cell formation in the amphipod crustacean Parhyale hawaiensis. Dev. Biol. 277, 387–402. (doi:10.1016/j.ydbio.2004.09.030. Crossref, PubMed, ISI, Google Scholar - 26
Roth S . 2004 Gastrulation in other insects. Gastrulation: from cells to embryos (ed.& Stern C. ), pp. 105–121. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. Google Scholar - 27
Rafiqi AM, Lemke S, Ferguson S, Stauber M& Schmidt-Ott U . 2008 Evolutionary origin of the amnioserosa in cyclorrhaphan flies correlates with spatial and temporal expression changes of zen. Proc. Natl Acad. Sci. USA 105, 234–239.doi:10.1073/pnas.0709145105 (doi:10.1073/pnas.0709145105). Crossref, PubMed, ISI, Google Scholar - 28
Schmidt-Ott U . 2000 The amnioserosa is an apomorphic character of cyclorrhaphan flies. Dev. Genes Evol. 210, 373–376.doi:10.1007/s004270000068 (doi:10.1007/s004270000068). Crossref, PubMed, ISI, Google Scholar - 29
Ferrar P . 1987 A guide to the breeding habits and immature stages of Diptera Cyclorrhapha. Leiden, The Netherlands: Brill u.a. Google Scholar - 30
Colless DH& McAlpine DK . 1970 Diptera. The insects of Australia (ed.& Waterhouse DF ), pp. 656–740. Carlton, Australia: Melbourne University Press. Google Scholar - 31
McAlpine JF . 1989 Manual of Nearctic Diptera. Ottawa, Canada: Research Branch, Agriculture Canada. Google Scholar - 32
Gibbs AG, Perkins MC& Markow TA . 2003 No place to hide: microclimates of Sonoran Desert Drosophila. J. Therm. Biol. 28, 353–362.doi:10.1016/S0306-4565(03)00011-1 (doi:10.1016/S0306-4565(03)00011-1). Crossref, ISI, Google Scholar - 33
Al-Saffar ZY, Grainger JNR& Aldrich J . 1995 Influence of constant and changing temperature and humidity on the development and survival of the eggs and pupae of Drosophila melanogaster (Meigen). J. Therm. Biol. 20, 389–397.doi:10.1016/0306-4565(94)00075-T (doi:10.1016/0306-4565(94)00075-T). Crossref, ISI, Google Scholar - 34
- 35
Goltsev Y, Rezende GL, Vranizan K, Lanzaro G, Valle D& Levine M . 2009 Developmental and evolutionary basis for drought tolerance of the Anopheles gambiae embryo. Dev. Biol. 330, 462–470.doi:10.1016/j.ydbio.2009.02.038 (doi:10.1016/j.ydbio.2009.02.038). Crossref, PubMed, ISI, Google Scholar - 36
Rezende GL, Martins AJ, Gentile C, Farnesi LC, Pelajo-Machado M, Peixoto AA& Valle D . 2008 Embryonic desiccation resistance in Aedes aegypti: presumptive role of the chitinized serosal cuticle. BMC Dev. Biol. 8, 82.doi:10.1186/1471-213x-8-82 (doi:10.1186/1471-213x-8-82). Crossref, PubMed, ISI, Google Scholar - 37
Furneaux PJS, James CR& Potter SA . 1969 The egg shell of the house cricket (Acheta domesticus): an electron-microscope study. J. Cell Sci. 5, 227–249. Crossref, PubMed, ISI, Google Scholar - 38
van der Zee M, Berns N& Roth S . 2005 Distinct functions of the Tribolium zerknullt genes in serosa specification and dorsal closure. Curr. Biol. 15, 624–636.doi:10.1016/j.cub.2005.02.057 (doi:10.1016/j.cub.2005.02.057). Crossref, PubMed, ISI, Google Scholar - 39
Panfilio KA . 2008 Extraembryonic development in insects and the acrobatics of blastokinesis. Dev. Biol. 313, 471–491.doi:10.1016/j.ydbio.2007.11.004 (doi:10.1016/j.ydbio.2007.11.004). Crossref, PubMed, ISI, Google Scholar - 40
Panfilio KA, Liu PZ, Akam M& Kaufman TC . 2006 Oncopeltus fasciatus zen is essential for serosal tissue function in katatrepsis. Dev. Biol. 292, 226–243.doi:10.1016/j.ydbio.2005.12.028 (doi:10.1016/j.ydbio.2005.12.028). Crossref, PubMed, ISI, Google Scholar - 41
Wakimoto BT, Turner FR& Kaufman TC . 1984 Defects in embryogenesis in mutants associated with the antennapedia gene-complex of Drosophila melanogaster. Dev. Biol. 102, 147–172.doi:10.1016/0012-1606(84)90182-9 (doi:10.1016/0012-1606(84)90182-9). Crossref, PubMed, ISI, Google Scholar - 42
Arakane Y, Hogenkamp DG, Zhu YC, Kramer KJ, Specht CA, Beeman RW, Kanost MR& Muthukrishnan S . 2004 Characterization of two chitin synthase genes of the red flour beetle, Tribolium castaneum, and alternate exon usage in one of the genes during development. Insect Biochem. Mol. Biol. 34, 291–304.doi:10.1016/j.ibmb.2003.11.004 (doi:10.1016/j.ibmb.2003.11.004). Crossref, PubMed, ISI, Google Scholar - 43
Arakane Y, Muthukrishnan S, Kramer KJ, Specht CA, Tomoyasu Y, Lorenzen MD, Kanost M& Beeman RW . 2005 The Tribolium chitin synthase genes TcCHS1 and TcCHS2 are specialized for synthesis of epidermal cuticle and midgut peritrophic matrix. Insect Mol. Biol. 14, 453–463.doi:10.1111/j.1365-2583.2005.00576.x (doi:10.1111/j.1365-2583.2005.00576.x). Crossref, PubMed, ISI, Google Scholar - 44
Arakane Y, Specht CA, Kramer KJ, Muthukrishnan S& Beeman RW . 2008 Chitin synthases are required for survival, fecundity and egg hatch in the red flour beetle, Tribolium castaneum. Insect Biochem. Mol. Biol. 38, 959–962.doi:10.1016/j.ibmb.2008.07.006 (doi:10.1016/j.ibmb.2008.07.006). Crossref, PubMed, ISI, Google Scholar - 45
Falciani F, Hausdorf B, Schroder R, Akam M, Tautz D, Denell R& Brown S . 1996 Class 3 Hox genes in insects and the origin of zen. Proc. Natl Acad. Sci. USA 93, 8479–8484.doi:10.1073/pnas.93.16.8479 (doi:10.1073/pnas.93.16.8479). Crossref, PubMed, ISI, Google Scholar - 46
Bucher G, Scholten J& Klingler M . 2002 Parental RNAi in Tribolium (Coleoptera). Curr. Biol. 12, R85–R86.doi:10.1016/S0960-9822(02)00666-8 (doi:10.1016/S0960-9822(02)00666-8). Crossref, PubMed, ISI, Google Scholar - 47
Akima H . 1978 Bivariate interpolation and smooth surface fitting for irregularly distributed data points. ACM Trans. Math. Softw. 4, 160–164.doi:10.1145/355780.355787 (doi:10.1145/355780.355787). Crossref, Google Scholar - 48
R Development Core Team. 2009 R: a language and environment for statistical computing (2.9.0 ed.). Vienna, Austria: R Foundation for Statistical Computing. Google Scholar
- 49
Winston PW& Bates DH . 1960 Saturated solutions for the control of humidity in biological research. Ecology 41, 232–237.doi:10.2307/1931961 (doi:10.2307/1931961). Crossref, ISI, Google Scholar - 50
Shippy TD, Ronshaugen M, Cande J, He JP, Beeman RW, Levine M, Brown SJ& Denell RE . 2008 Analysis of the Tribolium homeotic complex: insights into mechanisms constraining insect Hox clusters. Dev. Genes Evol. 218, 127–139.doi:10.1007/s00427-008-0213-4 (doi:10.1007/s00427-008-0213-4). Crossref, PubMed, ISI, Google Scholar - 51
Lamer A& Dorn A . 2001 The serosa of Manduca sexta (Insecta, Lepidoptera): ontogeny, secretory activity, structural changes, and functional considerations. Tissue Cell 33, 580–595.doi:10.1054/tice.2001.0213 (doi:10.1054/tice.2001.0213). Crossref, PubMed, ISI, Google Scholar - 52
Moussian B, Schwarz H, Bartoszewski S& Nusslein-Volhard C . 2005 Involvement of chitin in exoskeleton morphogenesis in Drosophila melanogaster. J. Morphol. 264, 117–130.doi:10.1002/jmor.10324 (doi:10.1002/jmor.10324). Crossref, PubMed, ISI, Google Scholar - 53
Schneider CA, Rasband WS& Eliceiri KW . 2012 NIH image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675.doi:10.1038/nmeth.2089 (doi:10.1038/nmeth.2089). Crossref, PubMed, ISI, Google Scholar - 54
Wieschaus E& Nusslein-Volhard C . 1986 Looking at embryos. Drosophila: a practical approach (ed.& Roberts DB ), pp. 199–227. Oxford, UK: IRL Press. Google Scholar - 55
Wright CS . 1984 Structural comparison of the two distinct sugar binding sites in wheat germ agglutinin isolectin II. J. Mol. Biol. 178, 91–104.doi:10.1016/0022-2836(84)90232-8 (doi:10.1016/0022-2836(84)90232-8). Crossref, PubMed, ISI, Google Scholar - 56
Solon J, Kaya-Çopur A, Colombelli J& Brunner D . 2009 Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure. Cell 137, 1331–1342.doi:10.1016/j.cell.2009.03.050 (doi:10.1016/j.cell.2009.03.050). Crossref, PubMed, ISI, Google Scholar - 57
Newcombe RG . 1998 Two-sided confidence intervals for the single proportion: comparison of seven methods. Stat. Med. 17, 857–872.doi:10.1002/(SICI)1097-0258(19980430)17:8%3C857::AID-SIM777%3E3.0.CO;2-E (doi:10.1002/(SICI)1097-0258(19980430)17:8<857::AID-SIM777>3.0.CO;2-E). Crossref, PubMed, ISI, Google Scholar - 58
Furneaux PJS& McFarlane JE . 1965 A possible relationship between the occurrence of catecholamines and water absorption in insect eggs. J. Insect Physiol. 11, 631–635.doi:10.1016/0022-1910(65)90145-9 (doi:10.1016/0022-1910(65)90145-9). Crossref, PubMed, Google Scholar - 59
Furneaux PJS& McFarlane JE . 1965 Identification, estimation, and localization of catecholamines in eggs of the house cricket, Acheta domesticus (L.). J. Insect Physiol. 11, 591–600.doi:10.1016/0022-1910(65)90141-1 (doi:10.1016/0022-1910(65)90141-1). Crossref, PubMed, Google Scholar - 60
McFarlane JE . 1960 Structure and function of the egg shell as related to water absorption by the eggs of Acheta domesticus (L.). Can. J. Zool. 38, 231–241.doi:10.1139/z60-029 (doi:10.1139/z60-029). Crossref, Google Scholar - 61
Reisz RR . 1997 The origin and early evolutionary history of amniotes. Trends Ecol. Evol. 12, 218–222.doi:10.1016/s0169-5347(97)01060-4 (doi:10.1016/s0169-5347(97)01060-4). Crossref, PubMed, ISI, Google Scholar - 62
Stewart WN . 1983 Paleobotany and the evolution of plants. New York, NY: Cambridge University Press. Google Scholar