Abstract
Eggs of the polyembryonic wasp Copidosoma floridanum undergo a clonal phase of proliferation, which results in the formation of thousands of embryos called secondary morulae and two castes called reproductive and soldier larvae. C. floridanum establishes the germ line early in development, and prior studies indicate that embryos with primordial germ cells (PGCs) develop into reproductive larvae while embryos without PGCs develop into soldiers. However, it is unclear how embryos lacking PGCs form and whether all or only some morulae contribute to the proliferation process. Here, we report that most embryos lacking PGCs form by division of a secondary morula into one daughter embryo that inherits the germ line and another that does not. C. floridanum embryos also incorporate 5-bromo-2′-deoxyuridine (BrdU), which allows PGCs and other cell types to be labeled during the S phase of the cell cycle. Continuous BrdU labeling indicated that all secondary morulae cycle during the proliferation phase of embryogenesis. Double labeling with BrdU and the mitosis marker anti-phospho-histone H3 indicated that the median length of the G2 phase of the cell cycle was 18 h with a minimum duration of 4 h. Mitosis of PGCs and presumptive somatic stem cells in secondary morulae was asynchronous, but cells of the inner membrane exhibited synchronous mitosis. Overall, our results suggest that all secondary morulae contribute to the formation of new embryos during the proliferation phase of embryogenesis and that PGCs are involved in regulating both proliferation and caste formation.
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References
Aherne WA, Camplejohn RS, Wright NA (1977) An introduction to cell population kinetics. Arnold, London
Baehrecke EH, Grbic M, Strand MR (1992) Serosa ontogeny in two embryonic morphs of Copidosoma floridanum, the influence of host hormones. J Exp Zool 262:30–39
Baehrecke EH, Aiken JM, Dover BA, Strand MR (1993) Ecdysteroid induction of embryonic morphogenesis in a parasitic wasp. Dev Biol 158:275–287
Buning J (1994) The insect ovary: ultrastructure, previtellogenic growth and evolution. Chapman and Hall, New York
Cheshier S, Morrison S, Liao X, Wissman I (1999) In vivo proliferation and cell cycle kinetics of long-term self-renewing hematopoietic stem cells. Proc Natl Acad Sci USA 96:3120–3125
Corley LS, White MT, Strand MR (2005) Both endogenous and environmental factors affect embryo proliferation in the polyembryonic wasp Copidosoma floridanum. Evol Dev 7:115–121
Cruz YP (1981) A sterile defender morph in a polyembryonic hymenopterous parasite. Nature 294:446–447
De Cuevas M, Lilly MA, Spradling AC (1997) Germline cyst formation in Drosophila. Annu Rev Genet 31:405–428
Dearden PK (2006) Germ cell development in the honeybee (Apis mellifera); Vasa and Nanos expression. BMC Dev Biol 6:6
Donnell DM, Corley LS, Chen G, Strand MR (2004) Inheritance of germ cells mediates caste determination in a polyembryonic wasp. Proc Natl Acad Sci USA 101:10095–10100
Extavour CG, Akam M (2003) Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130:5869–5884
Foe VE (1989) Mitotic domains reveal early commitment of cells in Drosophila embryos. Development 107:1–22
Gardiner EMM, Strand MR (2000) Hematopoiesis in larval Pseudoplusia includens and Spodoptera frugiperda. Arch Insect Biochem Physiol 43:147–164
Gardner A, Hardy ICW, Taylor PD, West SA (2007) Spiteful soldiers and sex ratio conflict in polyembryonic wasps. Am Nat 169:519–533
Gilbert LI, Rybczynski R, Warren JT (2002) Control and biochemical nature of the ecdysteroidogenic pathway. Annu Rev Entomol 47:883–912
Giron D, Strand MR (2004) Host resistance and the evolution of kin recognition in polyembryonic wasps. Proc R Soc Lond B Biol Sci 271:S395–S398
Giron D, Dunn D, Hardy ICW, Strand MR (2004) Aggression by polyembryonic wasp soldiers correlates with kinship but not resource competition. Nature 430:676–679
Giron D, Ross KG, Strand MR (2007) The presence of soldier larvae determines the outcome of competition in a polyembryonic wasp. J Evol Biol 20:165–172
Grbic M (2003) Polyembryony in parasitic wasps: evolution of a novel mode of development. Int J Dev Biol 47:633–642
Grbic M, Ode PJ, Strand MR (1992) Sibling rivalry and brood sex ratios in polyembryonic wasps. Nature 360:254–256
Grbic M, Nagy LM, Carroll SB, Strand M (1996) Polyembryonic development: insect pattern formation in a cellularized environment. Development 122:795–804
Grbic M, Nagy LM, Strand MR (1998) Development of polyembryonic insects: a major departure from typical embryogenesis. Dev Genes Evol 208:69–81
Harvey JA, Corley LS, Strand MR (2000) Competition induces adaptive shifts in caste ratios of a polyembryonic wasp. Nature 406:183–186
Hegner RW (1914) Studies on germ cells. J Morph 26:495–561
Hendzel MJ, Wei Y, Mancini MA, van Hooser A, Ranalli T, Brinkley BR, Bazett-Jones DP, Allis CD (1997) Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106:348–360
Ivanova-Kasas OM (1972) Polyembryony in insects. In: Counce S, Waddington CH (eds) Developmental systems, vol. 1. Insects. Academic, New York, pp 243–271
Lasko PF, Ashburner M (1988) The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A. Nature 335:611–617
Nijhout HF (2003) The control of body size in insects. Dev Biol 261:1–9
Ode PJ, Strand MR (1995) Progeny and sex allocation decisions of the polyembryonic wasp Copidosoma floridanum. J Anim Ecol 64:213–224
Patterson JT (1921) The development of Paracopidosomopsis. J Morph 36:1–69
Rabinovitch PS (1983) Regulation of human fibroblast growth rate by both noncycling cell fraction and transition probability is shown by growth in 5-bromodeoxyuridine followed by Hoechst 33258 flow cytometry. Proc Natl Acad Sci USA 80:2951–2955
Sander K (1996) Variants of embryonic patterning mechanisms in insects: Hymenoptera and Diptera. Semin Cell Dev Biol 7:573–582
Silvestri F (1937) Insect polyembryony and its general biological aspects. Bull Mus Comp Zool Harvard Univ 81:468–496
Sommer R, Tautz D (1991) Asynchronous mitotic domains during blastoderm formation in Musca domestica L. (Diptera) Roux's arch. Dev Biol 199:373–376
Strand MR (1989) Development of the polyembryonic parasitoid Copidosoma floridanum in Trichoplusia ni. Entomol Exp Appl 50:37–46
Strand MR (2009) Polyembryony. In: Carde R, Resch V (eds) Encyclopedia of insects, 2nd edn. Academic, New York, pp 928–932
Strand MR, Grbic M (1997) The development and evolution of polyembryonic insects. Curr Top Dev Biol 35:121–159
Truman JW, Bate M (1988) Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev Biol 125:145–157
Zhurov V, Terzin T, Grbic M (2004) Early blastomere determines embryo proliferation and caste fate in a polyembryonic wasp. Nature 43:764–769
Acknowledgements
We thank J. A. Johnson, M. Smith, and G. Chen for the assistance during the study. Funding for this project was provided by National Science Foundation Grant IOS 0414610 to MRS.
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Gordon, S.D., Strand, M.R. The polyembryonic wasp Copidosoma floridanum produces two castes by differentially parceling the germ line to daughter embryos during embryo proliferation. Dev Genes Evol 219, 445–454 (2009). https://doi.org/10.1007/s00427-009-0306-8
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DOI: https://doi.org/10.1007/s00427-009-0306-8