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Ecology and Evolution of Polyembryony

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Polyembryonic Insects

Part of the book series: Entomology Monographs ((ENTMON))

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Abstract

Sexual reproduction is the most common mode of reproduction in many multicellular organisms, including insects. The evolutionary success of sexual reproduction has been attributed to the generation of variation among offspring, which is important for the survival and future reproduction of the population. Consequently, populations that reproduce sexually can leave more offspring than those that reproduce asexually. This variation is created by the development of heritable mutations in the germ-cell lines in sexually reproducing organisms. These mutations are continuously reshuffled by the mixing and recombination of genes from two parents and are transferred to the next generation. More importantly, sexual reproduction will also eliminate accumulated, often harmful, alterations in the DNA that occur during meiosis and recombination—that is, individuals with harmful genes are unable to pass their genes to the next generation as a result of natural selection. On the other hand, the harmless portion of genes that are created during the process of meiosis from the harmful mutated genes may increase the chance of survival. By contrast, asexual reproduction results in the transfer of the full maternal genotype, which must be optimal in the present environment, and so asexually reproducing individual can successfully colonize new habitats and develop immediately (Williams 1975).

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References

  • Alford DV (1976) Observations on Litomastix aretas, an encyrtid parasite of the strawberry tortrix moth. Ann Appl Biol 84:1–5

    Article  Google Scholar 

  • Alié A, Leclere L, Jager M, Dayraud C, Chang P, Guyader HL, Queinnec E, M M (2011) Somatic stem cells express piwi and vasa genes in an adult ctenophore: ancient association of “germline genes” with stemness. Dev Biol 350:183–197

    Article  PubMed  CAS  Google Scholar 

  • Aoki S (1977) Colophina clematis (Homoptera, Pemphigidae), an aphid species with ‘soldiers’. Kontyu 45:276–282

    Google Scholar 

  • Avise JC (2015) Evolutionary perspectives on clonal reproduction in vertebrate animals. Proc Natl Acad Sci U S A 112:8867–8873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baehrecke EH, Strand MR (1990) Embryonic morphology and growth of the polyembryonic parasitoid Copidosoma floridanum (Ashmead) (Hymenoptera: Encyrtidae). Int J Insect Morphol Embryol 19:165–175

    Article  Google Scholar 

  • Baehrecke EH, Aiken JM, Dover BA, Strand MR (1993) Ecdysteroid induction of embryonic morphogenesis in a parasitic wasp. Dev Biol 158:275–287

    Article  CAS  PubMed  Google Scholar 

  • Birney EC, Baird DD (1985) Why do some mammals polyovulate to produce a litter of two? Am Nat 126:136–140

    Article  Google Scholar 

  • Bossdorf O, Richards CL, Pigliucci M (2008) Epigenetics for ecologists. Ecol Lett 11:106–115

    PubMed  Google Scholar 

  • Bowker CL, Ross KG, Strand MR (2014) The metabolic enzyme phosphoglucose isomerase (Pgi) affects the outcome of intra-specific competition in a polyembryonic wasp. Ecol Entomol 39:648–655

    Article  Google Scholar 

  • Bugler M, Rempoulakis P, Shacham R, Keasar T, Thuijsman F (2013) Sex allocation in a polyembryonic parasitoid with female soldiers: an evolutionary simulation and an experimental test. PLoS One 8:e64780

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Byers JR, Yu DS, Jones JW (1993) Parasitism of the army cutworm, Euxoa auxiliaris (Grt) (Lepidoptera, Noctuidae), by Copidosoma bakeri (Howard) (Hymenoptera, Encyrtidae) and effect on crop damage. Can Entomol 125:329–335

    Article  Google Scholar 

  • Charnov EL, Krebs JR (1974) On clutch-size and fitness. Ibis 116:217–219

    Article  Google Scholar 

  • Choe JC, Crespi BJ (1997) The evolution of social behavior in insects and arachnids. Cambridge University Press, London

    Book  Google Scholar 

  • Clausen CP (1972) Entomophagous insects. Hafner Publishing Company, New York. 688p

    Google Scholar 

  • Cook JM (1993) Sex determination in the Hymenoptera: a review of models and evidence. Heredity 71:421–435

    Article  Google Scholar 

  • Craig SF, Slobodkin LB, Wray G (1995) The ‘paradox’ of polyembryony. Trends Ecol Evol 10(9):371–372

    Article  CAS  PubMed  Google Scholar 

  • Craig SF, Slobodkin LB, Wray GA, Biermann CH (1997) The ‘paradox’ of polyembryony: a review of the cases and a hypothesis for its evolution. Evol Ecol 11:127–143

    Article  Google Scholar 

  • Crespi BJ (1992) Eusociality in Australian gall thrips. Nature 359:724–726

    Article  Google Scholar 

  • Crowley PH, Saeki Y (2009) Balancing the size-number tradeoff in clonal broods. Open Ecol J 2:100–111

    Article  Google Scholar 

  • Crowley PH, Saeki Y, Switzer PV (2009) Evolutionarily stable oviposition and sex ratio in parasitoid easps with single-sex broods. Ecol Entomol 34:163–175

    Article  Google Scholar 

  • Cruz YP (1981) A sterile defender morph in a polyembryonic hymenopterous parasite. Nature 294:446–477

    Article  Google Scholar 

  • Daniel DM (1932) Macrocentrus ancylivorus Rohwer, a polyembryonic braconid parasite of the oriental fruit moth. New York State Agric Exp Station Tech Bull 187:5–101

    Google Scholar 

  • Donnel DM (2014) Analysis of odorant-binding protein gene family members in the polyembryonic wasp, Copidosoma floridanum: evidence for caste bias and host interaction. J Insect Physiol 60:127–135

    Article  CAS  Google Scholar 

  • Donnell DM, Strand MR (2006) Caste-based differences in gene expression in the polyembryonic wasp Copidosoma floridanum. Insect Biochem Mol Biol 36:141–153

    Article  CAS  PubMed  Google Scholar 

  • Doutt RL (1947) Polyembryony in Copidosoma koehleri Blanchard. Am Nat 81:435–453

    Article  Google Scholar 

  • Dunn J, Dunn DW, Strand MR, Hardy IC (2017) Higher aggression towards closer relatives by soldier larvae in a polyembryonic wasp. Biol Lett 10:20140229

    Article  Google Scholar 

  • Enders AC (2002) Implantation in the nine-banded armadillo: how does a single blastocyst form four embryos? Placenta 23:71–85

    Article  CAS  PubMed  Google Scholar 

  • Fisher RA (1930) The genetical theory of natural selection. The Clarendon Press, Oxford

    Book  Google Scholar 

  • Fletcher DJC, Ross KG (1985) Regulation of reproduction in eusocial Hymenoptera. Annu Rev Entomol 30:19–43

    Article  Google Scholar 

  • Gadagkar R, Vinutha C, Shanubhogue A, Gore AP (1988) Pre-imaginal biasing of caste in a primitively eusocial insect. Proc R Soc B 233:175–189

    Google Scholar 

  • Galbreath GJ (1985) The evolution of monozygotic polyembryony in Dasypus. In: Montgomery GG (ed) The evolution and ecology of Armadillos, Sloths, and Vermilinguas. Smithsonian Institute Press, Washington, DC, pp 243–246

    Google Scholar 

  • Gardner A, West SA (2004a) Spite and the scale of competition. J Evol Biol 17:1195–1203

    Article  CAS  PubMed  Google Scholar 

  • Gardner A, West SA (2004b) Spite among siblings. Science 305:1413–1414

    Article  CAS  PubMed  Google Scholar 

  • Gardner A, Hardy IC, Taylor PD, West SA (2007) Spiteful soldiers and sex ratio conflict in polyembryonic parasitoid wasps. Am Nat 169:519–533

    Article  PubMed  Google Scholar 

  • Giron D, Harvey JA, Johnson JA, Strand MR (2007) Male soldier caste larvae are non-aggressive in the polyembryonic wasp. Biol Lett 3(4):431–434

    Article  PubMed  PubMed Central  Google Scholar 

  • Glastad KM, Chau LM, MAD G (2015) Epigenetics in social insects. Adv Insect Physiol 48:227–269

    Article  Google Scholar 

  • Gleeson SK, Clark AB, Dugatkin LA (1994) Monozygotic twinning: an evolutionary hypothesis. Proc Natl Acad Sci U S A 91:11363–11367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Godfray HCJ (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, Princeton

    Book  Google Scholar 

  • Gordon SD, Strand MR (2009) 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

    Article  PubMed  Google Scholar 

  • Grbic C (2003) Polyembryony in parasitic wasps: evolution of a novel mode of development. Int J Dev Biol 47:633–642

    PubMed  Google Scholar 

  • Grbic M, Ode PJ, Strand MR (1992) Sibling rivalry and brood sex ratios in polyembryonic wasps. Nature 360:254–256

    Article  Google Scholar 

  • Grbic M, Nagy LM, Carroll SB, Strand M (1996) Polyembryonic development: insect pattern formation in cellularized environment. Development 122:795–804

    CAS  PubMed  Google Scholar 

  • Grbic M, Rivers D, Strand M (1997) Caste formation in the polyembryonic wasp Copidosoma floridanum (Hymenoptera: Encyrtidae): in vivo and in vitro analysis. J Insect Physiol 43:553–565

    Article  CAS  PubMed  Google Scholar 

  • Grbic M, Nagy LM, Strand MR (1998) Development of polyembryonic insects: a major departure from typical insect embryogenesis. Dev Genes Evol 208:69–81

    Article  CAS  PubMed  Google Scholar 

  • Hamilton WD (1963) The evolution of altruistic behavior. Am Nat 97:354–356

    Article  Google Scholar 

  • Hamilton WD (1964) The genetical evolution of social behavior I. J Theor Biol 7:1–16

    Article  CAS  PubMed  Google Scholar 

  • Hamilton WD (1967) Extraordinary sex ratios. Science 156:477–488

    Article  CAS  PubMed  Google Scholar 

  • Hamilton WD (1970) Selfish and spiteful behavior in an evolutionary model. Nature 228:1218–1220

    Article  CAS  PubMed  Google Scholar 

  • Hardy ICW, Ode P, Strand MR (1993) Factors influencing brood sex ratios in polyembryonic Hymenoptera. Oecologia 93:343–348

    Article  PubMed  Google Scholar 

  • Hayashi Y, Lo N, Miyata H, Kitade O (2007) Sex-linked genetic influence on caste determination in a termite. Science 318:985–987

    Article  CAS  PubMed  Google Scholar 

  • Heiderer M, Westenberg C, Li D, Zhang H, Preiniger D, Dungl E (2018) Giant panda twin rearing without assistance requires more interactions and less rest of the mother—a case study at Vienna zoo. PLoS One 13:e0207433

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Heimpel GE, Rosenheim JA, Mangel M (1997) Predation on adult Aphytis parasitoids in the field. Oecologia 110:346–352

    Article  CAS  PubMed  Google Scholar 

  • Herre EA (1985) Sex ratio adjustment in fig wasps. Science 228:896–898

    Article  CAS  PubMed  Google Scholar 

  • Herre EA (1993) Population structure and the evolution of virulence in nematode parasites of fig wasps. Science 259:1442–1445

    Article  CAS  PubMed  Google Scholar 

  • Hoffmeister TS, Thiel A, Kock B, Babendreier D, Kuhlmann U (2000) Pre-patch experience affects the egg distribution pattern in a polyembryonic parasitoid of moth egg batches. Ethology 106:145–157

    Article  Google Scholar 

  • Holling CS (1959) Some characteristics of simple types of predation and parasitism. Can Entomol 91:385–398

    Article  Google Scholar 

  • Huxley JS, De Beer GR (1934) Experimental Embryony. Cambridge University Press, London

    Google Scholar 

  • Inoue H, Yoshimura J, Iwabuchi K, Barillas-Mury C (2014) Gene expression of protein-coding and non-coding RNAs related to Polyembryogenesis in the parasitic wasp, Copidosoma floridanum. PLoS One 9:e114372

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ivanova-Kasas OM (1961) Essays on the comparative embryology of Hymenoptera. Leningrad University Press, Leningrad. 266 pp

    Google Scholar 

  • Ivanova-Kasas OM (1972) Polyembryony in insects. In: Counce SJ, Waddington CH (eds) Developmental systems, vol 1. Academic Press, New York, pp 243–271

    Google Scholar 

  • Junnikkala E (1960) Life history and insect enemies of Hyponomeuta malinellus Zell. (Lep., Hyponomeutidae) in Finland. Ann Zool Soc Zool Bot Fenn Vanamo 21:3–44

    Google Scholar 

  • Keasar T, Segoli M, Steinberg R, Giron D, Strand MR, Bouskila A, Harari A (2006) Costs and consequences of superparasitism in the polyembryonic parasitoid Copidosoma koehleri (Hymenoptera: Encyrtidae). Ecol Entomol 31:277–283

    Article  Google Scholar 

  • Kent DS, Simpson JA (1992) Eusociality in the beetle Austroplatypus incompertus (Coleoptera: Curculionidae). Naturwissenschaften 79:86–87

    Article  Google Scholar 

  • King BH (1994) How do female parasitoid wasps assess host size during sex-ratio manipulation. Anim Behav 48:511–518

    Article  Google Scholar 

  • Kronforst MR, Gilley DC, Strassmann JE, Queller DC (2008) DNA methylation is widespread across social Hymenoptera. Curr Biol 18:R287–R288

    Article  CAS  PubMed  Google Scholar 

  • Kuhlmann U, Babendreier D, Hoffmeister TS, Mills NJ (1998) Impact and oviposition behavior of Ageniapsis fuscicollis (Hymenoptera: Encyrtidae), a polyembryonic parasitoid of the apple ermine moth., Yponomeuta malinellus (Lepidoptera: Yponomeutidae). Bull Entomol Res 88:617–625

    Article  Google Scholar 

  • Le Masurier AD (1987) A comparative study of the relationship between host size and brood size in Apanteles spp. (Hymenoptera: Braconidae). Ecol Entomol 12:383–393

    Article  Google Scholar 

  • Leiby RW (1926) The origin of mixed broods in polyembryonic Hymenoptera. Ann Entomological Society of America 19:290–299

    Article  Google Scholar 

  • Leiby RW, Hill CC (1923) The twinning and monembryonic development of Platygaster hiemalis, a parasite of the Hessian fly. J Agric Res 25:337–350

    Google Scholar 

  • Levitan DR, Petersen C (1995) Sperm limitation in the sea. Trends Ecol Evol 10:228–231

    Article  CAS  PubMed  Google Scholar 

  • Libbrecht R, Schwander T, Keller L (2011) Genetic components to caste allocation in a multiple-queen ant species. Evolution 65:2907–2915

    Article  PubMed  Google Scholar 

  • Loughry WJ, Prodöhl PA, McDonough CM, Avise JC (1998) Polyembryony in armadillos. Am Sci 86:274–279

    Article  Google Scholar 

  • Mani SR, Megosh H, Lin H (2014) PIWI proteins are essential for early Drosophila embryogenesis. Dev Biol 385:340–349

    Article  CAS  PubMed  Google Scholar 

  • Marchal P (1904) Recherches sur la biologie et le developpement des Hymenopteres parasites. Archives de zoologie expérimentale et générale 2:257–335

    Google Scholar 

  • Matsuura K, Vargo EL, Kawatsu K, Labadie PE, Nakano H, Yashiro T, Tsuji K (2009) Queen succession through asexual reproduction in termites. Science 323:1687

    Article  CAS  PubMed  Google Scholar 

  • Mayhew PJ, Glaizot O (2001) Integration theory of clutch size and body size evolution for parasitoids. Oikos 92:372–376

    Article  Google Scholar 

  • Michener CD (1969) Comparative social behavior of bees. Annu Rev Entomol 14:299–342

    Article  Google Scholar 

  • Mills NJ, Kuhlmann U (2004) Oviposition behavior of Trichogramma platneri Nagarkatti and Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae) in patches of single and clustered host eggs. Biol Control 30:42–51

    Article  Google Scholar 

  • Moleszka R (2008) Epigenetic integration of environmental and genomic signals in honey bees. Epigenetics 3:188–192

    Article  Google Scholar 

  • Morag N, Bouskila A, Harari A, Keasar T (2011a) Trans-generational effects of maternal rearing density on offspring development time in a parasitoid wasp. Physiol Entomol 36:294–298

    Article  Google Scholar 

  • Morag N, Harari AR, Bouskilla A, Keasar T (2011b) Low maternal host-encounter rate enhances offspring proliferation in a polyembryonic parasitoid. Behav Ecol Sociobiol 65:2287–2296

    Article  Google Scholar 

  • Morag N, Bouskila A, Rapp O, Segoli M, Keasar T, Harari AR (2011c) The mating status of mothers and offspring sex affect clutch size in a polyembryonic parasitoid wasp. Anim Behav 81:865–870

    Article  Google Scholar 

  • Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407

    Article  CAS  PubMed  Google Scholar 

  • O’Donnell S (1998) Reproductive caste determination in eusocial wasps (Hymenoptera: Vespidae). Annu Rev Entomol 43:323–346

    Article  PubMed  Google Scholar 

  • Ode PJ, Strand MR (1995) Progeny and sex allocation decisions of the polyembryonic wasp Copidosoma floridanum. J Anim Ecol 64:213–224

    Article  Google Scholar 

  • Ode PJ, Keasar T, Segoli M (2018) Lessons from the multitudes: insights from polyembryonic wasps for behavioral ecology. Curr Opin Insect Sci 27:32–37

    Article  PubMed  Google Scholar 

  • Ogata N, Yokoyama T, Iwabuchi K (2012) Transcriptome responses of insect fat body cells to tissue culture environment. PLoS One 7:e34940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton University Press, Princeton

    Google Scholar 

  • Otsuki T, Uka D, Ito H, Ichinose G, Nii M, Morita S, Sakamoto T, Nishiko M, Tabunoki H, Kobayashi K, Matsuura K, Iwabuchi K, Yoshimura J (2019) Mass killing by female soldier larvae is adaptive for the killed male larvae in a polyembryonic wasp. Sci Rep 9:7357

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Parker HL (1931) Macrocentrus gifuensis Ashmead, a polyembryonic braconid parasite in the European corn borer. USDA Tech Bull 230:1–63

    Google Scholar 

  • Patterson JT (1915) Observations on the development of Copidosoma gelechiae. Biol Bull 24:333–373

    Article  Google Scholar 

  • Patterson JT (1917) Studies of the biology of Paracopidosomopsis. I. Data on the sexes. Biol Bull 32:291–305

    Article  Google Scholar 

  • Patterson JT (1919) Polyembryony and sex. J Hered 10:344–352

    Article  Google Scholar 

  • Patterson JT (1927) Polyembryony in animals. Q Rev Biol 2:399–426

    Article  Google Scholar 

  • Rautiala P, Gardner A (2016) Intragenomic conflict over soldier allocation in polyembryonic parasitoid wasps. Am Nat 187:E106–E115

    Article  PubMed  Google Scholar 

  • Roff DA (2002) Life history evolution. Sinauer Associates, Inc., Sunderland

    Google Scholar 

  • Ryland JS (1996) Polyembryony ‘paradox’: the case of cyclostomate Bryozoa. Trends Ecol Evol 11:26

    Article  CAS  PubMed  Google Scholar 

  • Saeki Y, Crowley PH (2013) The size-number trade-off and components of fitness in clonal parasitoid broods. Entomol Exp Appl 149:241–249

    Article  Google Scholar 

  • Saeki Y, Crowley PH, Fox CW, Potter DA (2009) A sex-specific size-number tradeoff in clonal broods. Oikos 118:1552–1560

    Article  Google Scholar 

  • Salt G (1968) The resistance of insect parasitoids to the defence reactions of their hosts. Biol Rev Camb Philos Soc 43:200–232

    Article  CAS  PubMed  Google Scholar 

  • Schwager EE, Meng Y, Extavour CG (2015) Vasa and piwi are required for mitotic integrity in early embryogenesis in the spider Parasteatoda tepidariorum. Dev Biol 402:276–290

    Article  CAS  PubMed  Google Scholar 

  • Schwander T, Keller L (2008) Genetic compatibility affects queen and worker caste determination. Science 322:552–552

    Article  CAS  PubMed  Google Scholar 

  • Segoli M, Bouskila A, Harari AR, Keasar T (2009a) Developmental patterns in the polyembryonic parasitoid wasp Copidosoma koehleri. Arthropod Struct Dev 38:84–90

    Article  PubMed  Google Scholar 

  • Segoli M, Harari AR, Bouskila A, Keasar T (2009b) Brood size in a polyembryonic parasitoid wasp is affected by relatedness among competing larvae. Behav Ecol 20:761–767

    Article  Google Scholar 

  • Segoli M, Harari AR, Bouskila A, Keasar T (2009c) Host handling time in a polyembryonic wasp is affected both by previous experience and by host state (parasitized or not). J Insect Behav 22:501–510

    Article  Google Scholar 

  • Segoli M, Keasar T, Harari AR, Bouskila A (2009d) Limited kin discrimination abilities mediate tolerance toward relatives in polyembryonic parasitoid wasps. Behav Ecol 20:1262–1267

    Article  Google Scholar 

  • Segoli M, Keasar T, Bouskila A, Harari A (2010a) Host choice decisions in the polyembryonic wasp Copidosoma koehleri (Hymenoptera: Encyrtidae). Physiol Entomol 35:40–45

    Article  Google Scholar 

  • Segoli M, Harari AR, Bouskila A, Keasar T (2010b) The effect of host starvation on parasitoid brood size in a polyembryonic wasp. Evol Ecol Res 12:259–267

    Google Scholar 

  • Segoli M, Harari AR, Rosenheim JA, Bouskila A, Keasar T (2010c) The evolution of polyembryony in parasitoid wasps. J Evol Biol 23:1807–1819

    Article  CAS  PubMed  Google Scholar 

  • Shaham R, Ben-Shlomo R, Motro U, Keasar T (2016) Genom methylation patterns across castes and generations in a parasitoid wasp. Ecol Evol 6:7943–7953

    Article  PubMed  PubMed Central  Google Scholar 

  • Silvestri F (1937) Insect polyembryony and its general biological aspects. Bull Mus Comp Zool 81:469–498

    Google Scholar 

  • Skinner SW (1982) Maternally inherited sex ratio in the parasitoid wasp Nasonia vitripennis. Science 215:133–134

    Article  Google Scholar 

  • Slansky F Jr (1986) Nutritional ecology of endoparasitic insects and their hosts: an overview. J Insect Physiol 32:255–261

    Article  Google Scholar 

  • Smith CC, Fretwell SD (1974) The optimal balance between size and number of offspring. Am Nat 108:499–506

    Article  Google Scholar 

  • Smith MS, Milton I, Strand MR (2010) Phenotypically plastic traits regulate caste formation and soldier function in polyembryonic wasps. J Evol Biol 23:2677–2684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strand MR (1989a) Clutch size, sex ratio and mating by the polyembryonic encyrtid Copidosoma floridanum (Hymenoptera: Encyrtidae). Fla Entomol 72:32–42

    Article  Google Scholar 

  • Strand MR (1989b) Oviposition behavior and progeny allocation of the polyembryonic wasp Copidosoma floridanum (Hymenoptera: Encyrtidae). J Insect Behav 2:355–369

    Article  Google Scholar 

  • Strand MR (2003) Polyembryony. In: Carde R, Resch V (eds) Encyclopedia of insects. Academic Press, San Diego, pp 928–932

    Google Scholar 

  • Strand MR, Grbic M (1997a) The life history and development of polyembryonic parasitoids. In: Beckage NE (ed) Parasites and pathogens. Chapman & Hall, New York, pp 37–56

    Chapter  Google Scholar 

  • Strand MR, Grbic M (1997b) The development and evolution of polyembryonic insects. Curr Top Dev Biol 35:121–160

    Article  CAS  PubMed  Google Scholar 

  • Strand MR, Johnson JA, Culin JD (1990) Intrinsic interspecific competition between the polyembryonic parasitoid Copidosoma floridanum and solitary endoparasitoid Microplitis demolitor in Pseudoplusia includens. Entomol Exp Appl 55:275–284

    Article  Google Scholar 

  • Taylor PD (1981) Intra-sex and inter-sex sibling interactions as sex ratio determinants. Nature 291:64–66

    Article  Google Scholar 

  • Trivers RL, Hare H (1976) Haplodiploidy and the evolution of the social insects. Science 191:249–263

    Article  CAS  PubMed  Google Scholar 

  • Uka D, Hiraoka T, Iwabuchi K (2006) Physiological suppression of the larval parasitoid Glyptapanteles pallipes by the polyembryonic parasitoid Copidosoma floridanum. J Insect Physiol 52:1137–1142

    Article  CAS  PubMed  Google Scholar 

  • Uka D, Takahashi-Nakaguchi A, Yoshimura J, Iwabuchi K (2013) Male soldiers are functional in the Japanese strain of a polyembryonic wasp. Sci Rep 3:2312

    Article  PubMed  PubMed Central  Google Scholar 

  • Uka D, Sakamoto T, Yoshimura J, Iwabuchi K (2016) Sexual complementarity between host humoral toxicity and soldier caste in a polyembryonic wasp. Sci Rep 6:29336

    Article  PubMed  PubMed Central  Google Scholar 

  • Utsunomiya A, Iwabuchi K (2002) Interspecific competition between the polyembryonic wasp Copidosoma floridanum and the gregarious endoparasitoid Glyptapanteles pallipes. Entomol Exp Appl 104:353–362

    Article  Google Scholar 

  • van Alphen JJM, Visser ME (1990) Superparasitism as an adaptive strategy for insect parasitoids. Annu Rev Entomol 35:59–79

    Article  PubMed  Google Scholar 

  • Volkl W, Kroupa AS (1997) Effects of adult mortality risks on parasitoid foraging tactics. Anim Behav 54:349–359

    Article  Google Scholar 

  • Walter GH, Clarke AR (1992) Unisexual broods and sex ratios in a polyembryonic encyrtid parasitoid (Copidosoma sp.: hymenoptera). Oecologia 89:147–149

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Ye X, Shi M, Li F, Wang Z, Zhou Y, Gu Q, Wu X, Yin C, Guo D, Hu R, Hu N, Chen T, Zheng B, Zou J, Zhan L, Wei S, Wang Y, Huang J, Fang X, Strand MR, Chen X (2018) Parasitic insect-derived miRNAs modulate host development. Nat Commun 9:2205

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Weiblen GD (2002) How to be a fig wasp. Annu Rev Entomol 47:299–330

    Article  CAS  PubMed  Google Scholar 

  • Werren JH, Skinner SW, Vharnov EL (1981) Paternal inheritance of a daughterless sex ratio factor. Nature 293:467–468

    Article  Google Scholar 

  • Werren JH, Skinner SW, Huger AM (1986) Male killing bacteria in a parasitic wasp. Science 231:990–992

    Article  CAS  PubMed  Google Scholar 

  • West S (2009) Sex allocation. Princeton University Press, Princeton, NJ

    Book  Google Scholar 

  • Wheeler DE (1986) Developmental and physiological determinants of caste in social Hymenoptera: evolutionary implications. Am Nat 128:13–34

    Article  Google Scholar 

  • Williams GC (1966) Adaptation and natural selection. Princeton University Press, Princeton

    Google Scholar 

  • Williams GC (1975) Sex and evolution. Princeton University Press, Princeton

    Google Scholar 

  • Wilson EO (1971) The insect societies. Belknap, Harvard University Press, Cambridge

    Google Scholar 

  • Wilson EO (1985) The Sociogenesis of insect colonies. Science 228:1489–1495

    Article  CAS  PubMed  Google Scholar 

  • Yajima M, Wessel GM (2011) Small micromeres contribute to the germline in the sea urchin. Development 138:237–243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin C, Li M, Hu J, Lang K, Chen Q, Liu J, Guo D, He K, Dong Y, Luo J, Song Z, Walters JR, Zhang W, Li F, Chen X (2018) The genomic features of parasitism, polyembryony and immune evasion in the endoparasitic wasp Macrocentrus cingulum. BMC Genomics 19:420

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zappalà L, Hoy MA (2004) Reproductive strategies and parasitization behavior of Ageniaspis citricola, a parasitoid of the citrus leafminer Phyllocnistis citrella. Ann Entomol Soc Am 91:654–660

    Google Scholar 

  • Zhurov V, Terzin T, Grbic M (2004) Early blastomere determines embryo proliferation and caste fate in a polyembryonic wasp. Nature 432:746–769

    Article  CAS  Google Scholar 

  • Zhurov V, Terzin T, Grbić M (2007) (in)discrete charm of the polyembryony: evolution of embryo cloning. Cell Mol Life Sci 64:2790–2798

    Article  CAS  PubMed  Google Scholar 

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Iwabuchi, K. (2019). Ecology and Evolution of Polyembryony. In: Polyembryonic Insects. Entomology Monographs. Springer, Singapore. https://doi.org/10.1007/978-981-15-0958-2_5

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