Abstract
Decades have passed since the early molecular embryogenesis of Drosophila melanogaster was outlined. During this period, the molecular mechanisms underlying early embryonic development in other insects, particularly the flour beetle, Tribolium castaneum, have been described in more detail. The information clearly demonstrated that Drosophila embryogenesis is not representative of other insects and has highly distinctive characteristics. At the same time, this new data has been gradually clarifying ancestral operating mechanisms. The silk moth, Bombyx mori, is a lepidopteran insect and, as a representative of the order, has many unique characteristics found in early embryonic development that have not been identified in other insect groups. Herein, some of these characteristics are introduced and discussed in the context of recent information obtained from other insects.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
Not applicable.
References
Achtelig M, Krause G (1971) Experiments on uncleared egg of Pimpla turionellae L. (Hymenoptera) for functional analysis of oosome region. Wilhelm Roux Arch Entwickl Mech Org 167:164–182. https://doi.org/10.1007/BF00577038
Anderson DT (1972a) The development of hemimetabolous insects. In: Counce SJ, Waddington CH (eds) Developmental systems: insects, Vol.1. Academic Press, London, pp 95–163
Anderson DT (1972b) The development of holometabolous insects. In: Counce SJ, Waddington CH (eds) Developmental systems: insects, Vol.1. Academic Press, London, pp 165–242
Ansari S, Troelenberg N, Dao VA, Richter T, Bucher G, Klingler M (2018) Double abdomen in a short-germ insect: zygotic control of axis formation revealed in the beetle Tribolium castaneum. Proc Natl Acad Sci USA 116:1819–1824. https://doi.org/10.1073/pnas.1716512115
Barnett AA, Nakamura T, Extavour CG (2019) Hox genes limit germ cell formation in the short germ insect Gryllus bimaculatus. Proc Natl Acad Sci USA 115:16430–16435. https://doi.org/10.1073/pnas.1816024116
Benton MA, Pavlopoulos A (2014) Tribolium embryo morphogenesis: may the force be with you. Bioarchitecture 4:16–21. https://doi.org/10.4161/bioa.27815
Boos A, Distler J, Rudolf H, Klingler M, El-Sherif E (2018) A re-inducible gap gene cascade patterns the anterior–posterior axis of insects in a threshold-free fashion. eLife 7:e41208. https://doi.org/10.7554/eLife.41208
Bucher G, Klingler M (2004) Divergent segmentation mechanisms in the short germ insect Tribolium revealed by giant expression and function. Development 131:1729–1740. https://doi.org/10.1242/dev.01073
Carter J-M, Gibbs M, Breuker CJ (2015) Divergent RNA localisation patterns of maternal genes regulating embryonic patterning in the butterfly Pararge aegeria. PLoS ONE 10:e0144471. https://doi.org/10.1371/journal.pone.0144471
Cerny A, Bucher G, Schröder R, Klingler M (2005) Breakdown of abdominal patterning in the Tribolium Krüppel mutant jaws. Development 132:5353–5363. https://doi.org/10.1242/dev.02154
Chai CL, Zang Z, Huang FF, Wang XY, Yu QY (2008) A genomewide survey of homeobox genes and identification of novel structure of the Hox cluster in the silkworm Bombyx mori. Insect Biochem Mol Biol 38:1111–1120. https://doi.org/10.1016/j.ibmb.2008.06.008
Chang C-C, Dearden P, Akam M (2002) Germ line development in the grasshopper Schistocerca gregaria: vasa as a marker. Dev Biol 252:100–118. https://doi.org/10.1006/dbio.2002.0840
Chipman AD (2020) The evolution of the gene regulatory networks patterning the Drosophila blastoderm. Curr Top Dev Biol 139:297–324. https://doi.org/10.1016/bs.ctdb.2020.02.004
Choe CP, Miller SC, Brown SJ (2006) A pair-rule gene circuit defines segments sequentially in the short-germ insect Tribolium castaneum. Proc Natl Acad Sci USA 103:6560–6564. https://doi.org/10.1073/pnas.0510440103
Church SH, Donoughe S, de Medeiros BAS, Extavour CG (2019) Insect egg size and shape evolve with ecology but not developmental rate. Nature 571:58–62. https://doi.org/10.1038/s41586-019-1302-4
Clark E, Peel AD (2018) Evidence for the temporal regulation of insect segmentation by a conserved sequence of transcription factors. Development 145:155580. https://doi.org/10.1242/dev.155580
Clark E, Peel AD, Akam M (2019) Arthropod segmentation. Development 146:170480. https://doi.org/10.1242/dev.170480
Copf T, Schröder R, Averof M (2004) Ancestral role of caudal genes in axis elongation and segmentation. Proc Natl Acad Sci USA 101:17711–17715. https://doi.org/10.1073/pnas.0407327102
Davis GK, Patel NH (2002) Short, long, and beyond: molecular and embryological approaches to insect segmentation. Annu Rev Entomol 47:669–699. https://doi.org/10.1146/annurev.ento.47.091201.145251
Dearden PK (2006) Germ cell development in the Honeybee (Apis mellifera); vasa and nanos expression. BMC Dev Biol 6:6. https://doi.org/10.1186/1471-213X/6/6
Eddy M (1976) Germ plasm and the differentiation of the germ cell line. Int Rev Cytol 43:229–280. https://doi.org/10.1016/S0074-7696(08)60070-4
El-Sherif E, Averof M, Brown SJ (2012) A segmentation clock operating in blastoderm and germband stages of Tribolium development. Development 139:4341–4346. https://doi.org/10.1242/dev.085126
El-Sherif E, Zhu X, Fu J, Brown SJ (2014) Caudal regulates the spatiotemporal dynamics of pair-rule waves in Tribolium. PLoS Genet 10:e1004677. https://doi.org/10.1371/journal.pgen.1004677
Ephrussi A, Lehmann R (1992) Induction of germ cell formation by oskar. Nature 358:387–392. https://doi.org/10.1038/358387a0
Evans T, Wade CM, Chapman FA, Johnson AD, Loose M (2014) Acquisition of germ plasm accelerates vertebrate evolution. Science 344:200–203. https://doi.org/10.1126/science.1249325
Ewen-Campen B, Srouji JR, Schwager EE, Extavour CG (2012) Oskar predates the evolution of germ plasm in insects. Curr Bio 22:2278–2283. https://doi.org/10.1016/j.cub.2012.10.019
Extavour CG, Akam ME (2003) Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130:5869–5884. https://doi.org/10.1242/dev.00804
Ferguson L, Marlétaz F, Carter J-M, Taylor WR, Gibbs M, Breuker CJ, Holland PWH (2014) Ancient expansion of the Hox cluster in Lepidoptera generated four homeobox genes implicated in extra-embryonic tissue formation. PLoS Genet 10:e1004698. https://doi.org/10.1371/journal.pgen.1004698
Fleig R (1990) Engrailed expression and body segmentation in the honeybee Apis mellifera. Dev Genes Evol 198:467–473. https://doi.org/10.1007/BF00399057
Fu J, Posnien N, Bolognesi R, Fischer TD, Rayl P, Oberhofer G, Kitzmann P, Brown SJ, Bucher G (2012) Asymmetrically expressed axin required for anterior development in Tribolium. Proc Natl Acad Sci 109:7782–7786. https://doi.org/10.1073/pnas.1116641109
Gilbert SF (2000) The origins of anterior-posterior polarity. In: Developmental biology, 6th edn. Sinauer Associates, Sunderland (MA). https://www.ncbi.nlm.nih.gov/books/NBK10039/
Gorman MJ, Kankanala P, Kanost MR (2004) Bacterial challenge stimulates innate immune response in extraembryonic tissues of tobacco hornworm eggs. Insect Mol Biol 13:19–24. https://doi.org/10.1111/j.1365-2583.2004.00454.x
Hayashi Y, Hayashi M, Kobayashi S (2004) Nanos suppresses somatic cell fate in Drosophila germ line. Proc Natl Acad Sci USA 101:10338–10342. https://doi.org/10.1073/pnas.0401647101
Johnson AD, Alberio R (2015) Primordial germ cells: the first cell lineage or the last cells standing? Development 142:2730–2739. https://doi.org/10.1242/dev.113993
Johnson AD, Richardson E, Bachvarova RF, Crother BI (2011) Evolution of the germ line-soma relationship in vertebrate embryos. Reproduction 141:291–300. https://doi.org/10.1530/REP-10-0474
Kobayashi Y, Miya K (1987) Structure of egg cortex relating to presumptive embryonic and extraembryonic regions in silk-worm, Bombyx mori (Bombycidae: Lepidoptera). In: Ando H, Jura Cz (eds) Recent advances in insect embryology in Japan and Poland. ISEBU, Tsukuba, pp 181–194
Kotkamp K, Klingler M, Schoppmeier M (2010) Apparent role of Tribolium orthodenticle in anteroposterior blastoderm patterning largely reflects novel functions in dorsoventral axis formation and cell survival. Development 137:1853–1862. https://doi.org/10.1242/dev.047043
Kraft R, Jäckle H (1994) Drosophila mode of metamerization in the embryogenesis of the lepidopteran insect Manduca sexta. Proc Natl Acad Sci USA 91:6634–6638. https://doi.org/10.1073/pnas.91.14.6634
Liu W (2013) Bmdelta phenotype implies involvement of Notch signaling in body segmentation and appendage development in silkworm Bombyx mori. Arthropod Struct Dev 42:143–151. https://doi.org/10.1016/j.asd.2012.10.002
Liu PZ, Kaufman TC (2004) hunchback is required for suppression of abdominal identity, and for proper germband growth and segmentation in the intermediate germband insect Oncopeltus fasciatus. Development 131:1515–1527. https://doi.org/10.1242/dev.01046
Liu PZ, Kaufman TC (2005) Short and long germ segmentation: unanswered questions in the evolution of a developmental mode. Evol Dev 7(6):629–646. https://doi.org/10.1111/j.1525-142X.2005.05066.x
Lynch JA, Brent AE, Leaf DS, Pultz MA, Desplan C (2006) Localized maternal orthodenticle patterns anterior and posterior in the long germ wasp Nasonia. Nature 439:728–732. https://doi.org/10.1038/nature04445
Lynch JA, Ozuak O, Khila A, Abouhelf E, Desplan C, Roth S (2011) The phylogenetic origin of oskar coincided with the origin of maternally provisioned germ plasm and pole cells at the base of Holometabora. PLoS Genetics 7:e1002029. https://doi.org/10.1371/journal.pgen.1002029
Lynch JA, El-Sherif E, Brown SJ (2012) Comparisons of the embryonic development of Drosophila, Nasonia, and Tribolium. Wiley Interdiscip Rev Dev Biol 1:16–39. https://doi.org/10.1002/wdev.3
Marques-Souza H, Aranda M, Tautz D (2008) Delimiting the conserved features of hunchback function for the trunk organization of insects. Development 135:881–888. https://doi.org/10.1242/dev.018317
Mito T, Sarashina I, Zhang H, Iwahashi A, Okamoto H, Miyawaki K, Shinmyo Y, Ohuchi H, Noji S (2005) Non-canonical functions of hunchback in segment patterning of the intermediate germ cricket Gryllus bimaculatus. Development 132:2069–2079. https://doi.org/10.1242/dev.01784
Miya K (1958) Studies on the embryonic development of the gonad in the silkworm, Bombyx moriL. Part I. Differentiation of germ cells. J Fac Agric Iwate Univ 3:436–467
Miya K (1984) Early embryogenesis of Bombyx mori. In: King RC, Akai H (eds) Insect Ultrastructure, Vol.2. Plenum Publishing Corporation, pp 49–73
Myohara M (1994) Fate mapping of the silkworm, Bombyx mori, using localized irradiation of the egg at fertilization. Development 120:2869–2877. https://doi.org/10.1242/dev.120.10.2869
Nagoshi R (2008) Oogenesis. In: Capinera JL (ed) Encyclopedia of entomology. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-6359-6_1854
Nagy L, Riddiford L, Kiguchi K (1994) Morphogenesis in the early embryo of the Lepidopteran Bombyx mori. Dev Biol 165:137–151. https://doi.org/10.1006/dbio.1994.1241
Nakamura T, Extavour CG (2016) The transcriptional repressor Blimp-1 acts downstream of BMP signaling to generate primordial germ cells in the cricket Gryllus bimaculatus. Development 143:255–263. https://doi.org/10.1242/dev.127563
Nakamura T, Yoshizaki M, Ogawa S, Okamoto H, Shinmyo Y, Bando T, Ohuchi H, Noji S, MitoT (2010) Imaging of transgenic cricket embryos reveals cell movements consistent with a syncytial patterning mechanism. Curr Biol 20:1641–1647. https://doi.org/10.1016/j.cub.2010.07.044
Nakao H (1999) Isolation and characterization of a Bombyx vasa-like gene. Dev Genes Evol 209:312–316. https://doi.org/10.1007/as004270050257
Nakao H (2010) Characterization of Bombyx embryo segmentation process: expression profiles of engrailed, even skipped, caudal and wnt1/wingless homologues. J Exp Zool PartB Mol Dev Evol 314B:224–231. https://doi.org/10.1002/jez.b.21328
Nakao H (2012) Anterior and posterior centers jointly regulate Bombyx embryo body segmentation. Dev Biol 371:293–301. https://doi.org/10.1016/j.ydbio.2012.08.029
Nakao H (2015) Analyses of interactions among pair-rule genes and the gap gene Krüppel in Bombyx segmentation. Dev Biol 371:293–301. https://doi.org/10.1016/j.ydbio.2015.06.012
Nakao H (2016) Hunchback knockdown induces supernumerary segment formation in Bombyx. Dev Biol 413:207–216. https://doi.org/10.1016/j.ydbio.2016.03.024
Nakao H (2018) A Bombyx homolog of ovo is a segmentation gene that acts downstream of Bm-wnt1 (Bombyx wnt1 homolog). Gene Expr patterns 27:1–7. https://doi.org/10.1016/j.gep.2017.10.002
Nakao H, Takasu Y (2019) Complexities in Bombyx germ cell formation process revealed by Bm-nosO (a Bombyx homolog of nanos) knockout. Dev Biol 445:29–36. https://doi.org/10.1016/j.ydbio.2018.10.012
Nakao H, Hatakeyama M, Lee JM, Shimoda M, Kanda T (2006) Expression pattern of Bombyx vasa-like (BmVLG) protein and its implications in germ cell development. Dev Genes Evol 216:94–99. https://doi.org/10.1007/s00427-005-0033-8
Nakao H, Matsumoto T, Oba Y, Niimi T, Yaginuma T (2008) Germ cell specification and early embryonic patterning in Bombyx mori as revealed by nanos orthologues. Evol Dev 10:546–554. https://doi.org/10.1111/j.1525-142X.2008.00270.x
Oates AC, Morelli LG, Ares S (2012) Patterning embryos with oscillations: structure, function and dynamics of the vertebrate segmentation clock. Development 139:625–639. https://doi.org/10.1242/dev.063735
Ohinata Y, Ohta H, Shigeta M, Yamanaka K, Wakayama T, Saitou M (2009) A signaling principle for the specification of the germ cell lineage in mice. Cell 137:571–584. https://doi.org/10.1016/j.cell.2009.03.014
Olesnicky EC, Brent AE, Tonnes L, Walker M, Pultz MA, Leaf D, Desplan C (2006) A caudal mRNA gradient controls posterior development in the wasp Nasonia. Development 133:3973–3982. https://doi.org/10.1242/dev.02576
Overton PM, Chia W, Buescher M (2007) The Drosophila HMG-domain proteins SoxNeuro and Dichaete direct trichome formation via the activation of shavenbaby and the restriction of Wingless pathway activity. Development 134:2807–2813. https://doi.org/10.1242/dev.02878
Pankratz MJ, Jäckle H (1993) Blastoderm segmentation. In: Bate M, Arias AM (eds) The development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, New York, pp 467–516
Patel NH, Hayward DC, Lall S, Pirkl NR, DiPietro D, Ball EE (2001) Grasshopper hunchback expression reveals conserved and novel aspects of axis formation and segmentation. Development 128:3459–3472. https://doi.org/10.1242/dev.128.18.3459
Pechmann M, Kenny NJ, Pott L, Heger P, Chen Y-T, Buchta T, Özüak O, Lynch J, Roth S (2021) Striking parallels between dorsoventral patterning in Drosophila and Gryllus reveal a complex evolutionary history behind a model gene regulatory network. eLife 10:e68287. https://doi.org/10.7554/eLife.68287
Peel AD (2008) The evolution of developmental gene networks: lessons from comparative studies on hoplometabolous insects. Phil Trans R Soc B 363:1539–1547. https://doi.org/10.1098/rstb.2007.22144
Peel AD, Chipman AD, Akam M (2005) Arthropod segmentation: beyond the Drosophila paradigm. Nat Rev Genet 6:905–916. https://doi.org/10.1038/nrg1724
Pultz MA, Westendorf L, Gale SD, Hawkins K, Lynch J, Pitt JN, Reeves NL, Yao JCY, Small S, Desplan C, Leaf DS (2005) A major role for zygotic hunchback in patterning the Nasonia embryo. Development 132:3705–3715. https://doi.org/10.1242/dev.01939
Roth S, Lynch JA (2009) Symmetry breaking during Drosophila oogenesis. Cold Spring Harb Perspect Biol 1:e001891. https://doi.org/10.1101/cshperspect.a001891
Rudolf H, Zellner C, El-Sherif E (2020) Speeding up anterior-posterior patterning of insects by differential initialization of the gap gene cascade. Dev Biol 460:20–31. https://doi.org/10.1016/j.ydbio.2019.04.015
Sander K (1976) Specification of the basic body pattern in insect embryogenesis. Adv Insect Physiol 12:125–238. https://doi.org/10.1016/S0065-2806(08)60255-6
Sarrazin AF, Peel AD, Averof MA (2012) Segmentation clock with two-segment periodicity in insects. Science 336:338–341. https://doi.org/10.1126/science.1218256
Schinko JB, Kreuzer N, Offen N, Posnien N, Wimmer EA, Bucher G (2008) Divergent functions of orthodenticle, empty spiracles and buttonhead in early head patterning of the beetle Tribolium castaneum (Coleoptera). Dev Biol 317:600–613. https://doi.org/10.1016/j.ydbio.2008.03.005
Schmitt-Engel C, Cerny AC, Schoppmeier M (2012) A dual role for nanos and pumilio in anterior and posterior blastodermal patterning of the short-germ beetle Tribolium castaneum. Dev Biol 364:224–235. https://doi.org/10.1016/j.ydbio.2012.01.024
Schröder R (2006) vasa mRNA accumulates at the posterior pole during blastoderm formation in the flour beetle Tribolium castaneum. Dev Genes Evol 216:277–283. https://doi.org/10.1007/s00427-005-0054-3
Shinmyo Y, Mito T, Matsushita T, Sarashina I, Miyawaki K, Ohuchi H, Noji S (2005) caudal is required for gnathal and thoracic patterning and for posterior elongation in the intermediate-germband cricket Gryllus bimaculatus. Mech Dev 122:231–239. https://doi.org/10.1016/j.mod.2004.10.001
Simpson-Brose M, Treisman J, Desplan C (1994) Synergy between the hunchback and bicoid morphogens is required for anterior patterning in Drosophila. Cell 78:855–865. https://doi.org/10.1016/s0092-8674(94)90622-x
St Johnston D (1993) Pole plasm and the posterior group genes. In: Bate M, Arias AM (eds) The development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, New York, pp 325–363
Stein DS, Stevens LM (2014) Maternal control of the Drosophila dorsal–ventral body axis. WIREs Dev.Biol 3:301–330. https://doi.org/10.1002/wdev.138
Takesue S, Keino H, Onitake K (1980) Blastoderm formation in the silkworm egg (Bombyx mori L). J Embryol Exp Morph 60:117–124
Tautz D (2004) Segmentation. Dev Cell 7:301–312. https://doi.org/10.1016/j.devcel.2004.08.008
van der Zee M, Berns N, Roth S (2005) Distinct functions of the Tribolium zerknüllt genes in serosa specification and dorsal closure. Curr Biol 15:624–636. https://doi.org/10.1016/j.cub.2005.02.057
Whittle CA, Extavour CG (2017) Causes and evolutionary consequences of primordial germ-cell specification mode in metazoans. Proc Natl Acad Sci USA 114:5784–5791. https://doi.org/10.1073/pnas.1610600114
Williams TA, Nagy LM (2017) Linking gene regulation to cell behaviors in the posterior growth zone of sequentially segmenting arthropods. Arthropod Struct Dev 46:380–394. https://doi.org/10.1016/j.asd.2016.10.003
Wilson MJ, Dearden PK (2011) Diversity in insect axis formation: two orthodenticle genes and hunchback act in anterior patterning and influence dorsoventral organization in the honeybee (Apis mellifera). Development 138:3497–3507. https://doi.org/10.1242/dev.067926
Wilson MJ, Havler M, Dearden PK (2010a) Giant, Krüppel, and caudal act as gap genes with extensive roles in patterning the honeybee embryo. Dev Biol 339:200–211. https://doi.org/10.1016/j.ydbio.2009.12.015
Wilson MJ, McKelvey BH, van der Heide S, Dearden PK (2010b) Notch signaling does not regulate segmentation in the honeybee, Apis mellifera. Dev Genes Evol 220:179–190. https://doi.org/10.1007/s00427-010-0340-6
Wipfler B, Letsch H, Frandsen PB, Kapli P, Mayer C, Bartel D, Buckley TR, Donath A, Edgerly-Rooks JS, Fujita M, Liu S, Machida R, Mashimo Y, Misof B, Niehuis O, Peters RS, Petersen M, Podsiadlowski L, Schutte K, Shimizu S et al (2019) Evolutionary history of polyneoptera and its implications for our understanding of early winged insects. Proc Natl Acad Sci USA 116:3024–3029. https://doi.org/10.1073/pnas.1817794116
Wolff C, Sommer R, Schröder R, Glaser G, Tautz D (1995) Conserved and divergent expression aspects of the Drosophila segmentation gene hunchback in the short germ band embryo of the flour beetle Tribolium. Development 121:4227–4236. https://doi.org/10.1242/dev.121.12.4227
Xu X, Xu PX, Amanai K, Suzuki Y (1997) Double-segment defining role of even-skipped homologs along the evolution of insect pattern formation. Dev Growth Differ 39:515–522. https://doi.org/10.1046/j.1440-169X.1997.t01-3-00013.x
Zhu X, Rudolf H, Healey L, François P, Brown SJ, Klingler M, El-Sherif E (2017) Speed regulation of genetic cascades allows for evolvability in the body plan specification of insects. Proc Natl Acad Sci:E8646–E8655. https://doi.org/10.1073/pnas.1702478114
Acknowledgements
I greatly thank the anonymous reviewers for their valuable comments and discussions. The author also would like to thank Enago (www.enago.jp) for the English language review.
Code availability
Not applicable.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Conflict of interest
The authors declare no competing interests.
Additional information
Communicated by Nico Posnien
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Nakao, H. Early embryonic development of Bombyx. Dev Genes Evol 231, 95–107 (2021). https://doi.org/10.1007/s00427-021-00679-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00427-021-00679-8