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Journal of Integrative Agriculture  2020, Vol. 19 Issue (6): 1447-1457    DOI: 10.1016/S2095-3119(19)62767-X
Special Focus: Physiology and interaction of insects with environmental factors Advanced Online Publication | Current Issue | Archive | Adv Search |
Reproductive polyphenism and its advantages in aphids: Switching between sexual and asexual reproduction
YAN Shuo1, WANG Wan-xing2, SHEN Jie1 
1 Department of Entomology/MOA Key Lab of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural University, Beijing 100193, P.R.China
2 Key Lab of Biology and Genetic Improvement of Root and Tuber Crops, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
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Reproductive polyphenism, which allows one genotype to produce sexual and asexual morphs, is an extreme case of phenotypic plasticity and is commonly observed in aphids.  Aphids are typical species that switch these reproductive modes, and the pathway orientation is triggered by the environmental conditions (mainly photoperiod and temperature).  The typical annual life of aphids includes a succession of parthenogenetic generations during the spring and summer and a single sexual generation in autumn.  In this review, we describe how the environmental cues orientate the reproductive mode of aphids from photoperiodic perception to endocrine regulation, and how juvenile hormones may act on the target cells (oocytes) to initiate the gametogenesis and embryogenesis in sexual and asexual reproduction.  We also discuss the paradox of sex, especially the advantages of sexual reproduction in aphids.  With the recent development of genomic resources in aphids, many potential genes involved in the reproductive polyphenism will enter the public’s awareness.  In particular, we describe a novel RNAi method in aphids, which may provide a molecular technique for determining the developmental fate and multiple reproductive strategies.
Keywords:  aphids        parthenogenesis        embryogenesis        gametogenesis        photoperiodism  
Received: 06 May 2019   Accepted:
Fund: This work was supported by the National Key Research and Development Program of China (2018YFD0200804 and 2017YFD0201200).
Corresponding Authors:  Correspondence SHEN Jie, E-mail:   
About author:  YAN Shuo, E-mail:;

Cite this article: 

YAN Shuo, WANG Wan-xing, SHEN Jie. 2020. Reproductive polyphenism and its advantages in aphids: Switching between sexual and asexual reproduction. Journal of Integrative Agriculture, 19(6): 1447-1457.

Allen M L, Walker W B Ⅲ. 2012. Saliva of Lygus lineolaris digests double stranded ribonucleic acids. Journal of Insect Physiology, 58, 391–396.
Beekman M, Allsopp M H, Lim J, Goudie F, Oldroyd B P. 2011. Asexually produced cape honeybee queens (Apis mellifera capensis) reproduce sexually. Journal of Heredity, 102, 562–566.
Beldade P, Mateus A R A, Keller R A. 2011. Evolution and molecular mechanisms of adaptive developmental plasticity. Molecular Ecology, 20, 1347–1363.
Bermingham J, Wilkinson T. 2009. Embryo nutrition in parthenogenetic viviparous aphids. Physiological Entomology, 34, 103–109.
Blackman R L. 1974. Life-cycle variation of Myzus persicae (Sulz.) (Hem., Aphididae) in different parts of the world, in relation to genotype and environment. Bulletin of Entomological Research, 63, 595–607.
Bulmer M G. 1982. Cyclical parthenogenesis and the cost of sex. Journal of Theoretical Biology, 94, 197–207.
Büning J. 1985. Morphology, ultrastructure, and germ cell cluster formation in ovarioles of aphids. Journal of Morphology, 186, 209–221.
Campbell C A M, Tregidga E. 2005. Photoperiodic determination of gynoparae and males of damson-hop aphid Phorodon humuli. Physiological Entomology, 30, 189–194.
Chang C C, Lee W C, Cook C E, Lin G W, Chang T. 2006. Germ-plasm specification and germline development in the parthenogenetic pea aphid Acyrthosiphon pisum: Vasa and nanos as markers. International Journal of Developmental Biology, 50, 413–421.
Chang C C, Lin G W, Cook C E, Horng S B, Lee H J, Huang T Y. 2007. Apvasa marks germ-cell migration in the parthenogenetic pea aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). Development Genes and Evolution, 217, 275–287.
Chen F J, Wu G, Ge F. 2004. Impacts of elevated CO2 on the population abundance and reproductive activity of aphid Sitobion avenae Fabricius feeding on spring wheat. Journal of Applied Entomology, 128, 723–730.
Christiaens O, Smagghe G. 2014. The challenge of RNAi-mediated control of hemipterans. Current Opinion in Insect Science, 6, 15–21.
Christiaens O, Swevers L, Smagghe G. 2014. DsRNA degradation in the pea aphid (Acyrthosiphon pisum) associated with lack of response in RNAi feeding and injection assay. Peptides, 53, 307–314.
Corbitt T S, Hardie J. 1985. Juvenile hormone effects on polymorphism in the pea aphid, Acyrthosiphon pisum. Entomologia Experimentalis et Applicata, 38, 131–135.
Cortés T, Tagu D, Simon J C, Moya A, Martínez-Torres D. 2008. Sex versus parthenogenesis: a transcriptomic approach of photoperiod response in the model aphid Acyrthosiphon pisum (Hemiptera: Aphididae). Gene, 408, 146–156.
Dedryver C A, Hullé M, Le Gallic J F, Caillaud M C, Simon J C. 2001. Coexistence in space and time of sexual and asexual populations of the cereal aphid Sitobion avenae. Oecologia, 128, 379–388.
Delmotte F, Leterme N, Gauthier J P, Rispe C, Simon J C. 2002. Genetic architecture of sexual and asexual populations of the aphid Rhopalosiphum padi based on allozyme and microsatellite markers. Molecular Ecology, 11, 711–723.
Emlen D J, Nijout H F. 1999. Hormonal control of male horn length dimorphism in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae). Journal of Insect Physiology, 45, 45–53.
Fenton B, Woodford J A T, Malloch G. 1998. Analysis of clonal diversity of the peach-potato aphid, Myzus persicae (Sulzer), in Scotland, UK and evidence for existence of a predominant clone. Molecular Ecology, 7, 1475–1487.
Forrest J M S. 1970. The effect of maternal and larval experience on morph determination in Dysaphis devecta. Journal of Insect Physiology, 16, 2281–2292.
Fournier D, Estoup A, Orivel J, Foucaud J, Jourdan H, Le Breton J, Keller L. 2005. Clonal reproduction by males and females in the little fire ant. Nature, 435, 1230–1234.
Frantz A, Plantegenest M, Simon J C. 2006. Temporal habitat variability and the maintenance of sex in host populations of the pea aphid. Proceedings of the Royal Society (B: Biological Sciences), 273, 2887–2891.
Gao N, Foster R G, Hardie J. 2000. Two opsin genes from the vetch aphid, Megoura viciae. Insect Molecular Biology, 9, 197–202.
Gao N, Hardie J. 1997. Melatonin and pea aphid, Acyrthosiphon pisum. Journal of Insect Physiology, 43, 615–620.
Gao N, Von Schantz M, Foster R G, Hardie J. 1999. The putative brain photoperiodic photoreceptors in the vetch aphid, Megoura viciae. Journal of Insect Physiology, 45, 1011–1019.
Gerber H S, Klostermeyer E C. 1970. Sex control by bees: A voluntary act of egg fertilization during oviposition. Science, 167, 82–84.
Gilbert S F. 2001. Ecological developmental biology: developmental biology meets the real world. Developmental Biology, 233, 1–12.
Gómez A, Carvalho G R. 2000. Sex, parthenogenesis and genetic structure of rotifers: microsatellite analysis of contemporary and testing egg bank populations. Molecular Ecology, 9, 203–214.
Guo H, Sun Y, Li Y, Tong B, Harris M, Zhu-Salzman K, Ge F. 2013. Pea aphid promotes amino acid metabolism both in Medicago truncatula and bacteriocytes to favor aphid population growth under elevated CO2. Global Change Biology, 19, 3210–3223.
Haack L, Simon J C, Gauthier J P, Plantegenest M, dedryver C A. 2000. Evidence for predominant clones in a cyclically parthenogenetic organism provided by combined demographic and genetic analyses. Molecular Ecology, 9, 2055–2066.
Hales D F, Tomiuk J, Wöhrmann K, Sunnucks P. 1997. Evolutionary and genetic aspects of aphid biology: A review. European Journal of Entomology, 94, 1–55.
Hamilton G A. 1953. Thelytokous parthenogenesis for four generations in the desert locust (Schistocerca gregaria Forsk). Nature, 173, 1153–1154.
Hardie J. 1987a. The corpus allatum, neurosecretion and photoperiodically controlled polymorphism in an aphid. Journal of Insect Physiology, 33, 201–205.
Hardie J. 1987b. Juvenile hormone stimulation of oocyte development and embryogenesis in the parthenogenetic ovaries of an aphid, Aphis fabae. International Journal of Invertebrate Reproduction and Development, 11, 189–202.
Hardie J. 1990. The photoperiodic counter, quantitative day-length effects and scotophase timing in the vetch aphid Megoura viciae. Journal of Insect Physiology, 36, 939–949.
Hardie J, Baker F C, Jamieson G C, Lees A D, Schooley D A. 1985. The identification of an aphid juvenile hormone, and its titre in relation to photoperiod. Physiological Entomology, 10, 297–302.
Hardie J, Lees A D. 1985. The induction of normal and teratoid viviparae by a juvenile hormone and kinoprene in two species of aphids. Physiological Entomology, 10, 65–74.
Hardie J, Lees A D, Young S. 1981. Light transmission through the head capsule of an aphid, Megoura viciae. Journal of Insect Physiology, 27, 773–775.
He B, Chu Y, Yin M, Müllen K, An C, Shen J. 2013. Fluorescent nanoparticle delivered dsRNA toward genetic control of insect pests. Advanced Materials, 25, 4580–4584.
Ishikawa A, Ogawa K, Gotoh H, Walsh T K, Tagu D, Brisson J A, Rispe C, Jaubert-Possamai S, Kanbe T, Tsubota T, Shiotsuki T, Miura T. 2012. Juvenile hormone titre and related gene expression during the change of reproductive modes in the pea aphid. Insect Molecular Biology, 21, 49–60.
Kanbe T, Akimoto S I. 2009. Allelic and genotypic diversity in long-term asexual populations of the pea aphid, Acyrthosiphon pisum in comparison with sexual populations. Molecular Ecology, 18, 801–816.
Kelber A, Vorobyev M, Osorio D. 2003. Animal colour vision-behavioural tests and physiological concepts. Biological Reviews of the Cambridge Philosophical Society, 78, 81–118.
Lachowska D, Ro?ek M, Holecová M. 2008. New data on the cytology of parthenogenetic weevils (Coleoptera, Curculionidae). Genetica, 134, 235–242.
Lamb R J, Pointing P J. 1972. Sexual morph determination in the aphid, Acyrthosiphon pisum. Journal of Insect Physiology, 18, 2029–2042.
Langham G. 2004. Specialized avian predators repeatedly attack novel color morphs of Heliconius butterflies. Evolution, 58, 2783–2787.
Lees A D. 1964. The location of the photoperiodic receptors in the aphid Megoura viciae Buckton. Journal of Experimental Biology, 41, 119–133.
Lees A D. 1973. Photoperiodic time measurement in the aphid Megoura viciae. Journal of Insect Physiology, 19, 2279–2316.
Li H, Yan S, Li Z, Zhang Q, Liu X. 2015. Dim light during scotophase enhances sexual behavior of the oriental tobacco budworm Helicoverpa assulta (Lepidoptera: Noctuidae). Florida Entomologist, 98, 690–696.
Little C J, Chapuis M P, Blondin L, Chapuis E, Jourdan-Pineau H. 2017. Exploring the relationship between tychoparthenogenesis and inbreeding depression in the desert locust, Schistocerca gregaria. Ecology and Evolution, 7, 6003–6011.
Liu K, Xu Z, Yin M, Yang W, He B, Wei W, Shen J. 2014. A multifunctional perylenediimide derivative (DTPDI) can be used as a recyclable specific Hg2+ ion sensor and an efficient DNA delivery carrier. Journal of Materials Chemistry (B), 2, 2093–2096.
Liu Y J, Yan S, Shen Z J, Li Z, Zhang X F, Liu X M, Zhang Q W, Liu X X. 2018. The expression of three opsin genes and phototactic behavior of Spodoptera exigua (Lepidoptera: Noctuidae): evidence for visual function of opsin in phototaxis. Insect Biochemistry and Molecular Biology, 96, 27–35.
Mandrioli M, Zanetti E, Nardelli A, Manicardi G C. 2018. Potential role of the heat shock protein 90 (hsp90) in buffering mutations to favour cyclical parthenogenesis in the peach potato aphid Myzus persicae (Aphididae, Hemiptera). Bulletin of Entomological Research, doi: 0.1017/S0007485318000688
Marcovitch S. 1923. Plant lice and light exposure. Science, 58, 537–538.
Marcovitch S. 1924. The migration of the aphididae and the appearance of the sexual forms as affected by the relative length of daily light exposure. Journal of Agricultural Research, 27, 513–522.
Margaritopoulos J T, Tsitsipis J A. 2002. Production of sexual morphs by apterous virginoparae of Myzus persicae (Hemiptera: Aphididae) in relation to pre- and postnatal exposure to short day conditions. Bulletin of Entomological Research, 92, 321–330.
Matsuka M, Mittler T E. 1979. Production of males and gynoparae by apterous viviparae of Myzus persicae continuously exposed to different scotoperiods. Journal of Insect Physiology, 25, 587–593.
Matsuura K, Vargo E L, Kawatsu K, Labadie P E, Nakano H, Yashiro T, Tsuji K. 2009. Queen succession through asexual reproduction in termites. Science, 323, 1687.
Mittler T E, Eisenbach J, Searle J B, Matsuka M, Nassar S G. 1979. Inhibition by kinoprene of photoperiod-induced male production by apterous and alate viviparae of the aphid Myzus persicae. Journal of Insect Physiology, 25, 219–226.
Mittler T E, Nassar S G, Staal G B. 1976. Wing development and parthenogenesis induced in progenies of kinoprene-treated gynoparae of Aphis fabae and Myzus persicae. Journal of Insect Physiology, 22, 1717–1725.
Miura T. 2005. Developmental regulation of caste-specific characters in social-insect polyphenism. Evolution and Development, 7, 122–129.
Miura T, Braendle C, Shingleton A, Sisk G, Kambhampati S, Stern D L. 2003. A comparison of parthenogenetic and sexual embryogenesis of the pea aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). Journal of Experimental Zoology Molecular and Developmental Evolution, 295, 59–81.
Moczek A P. 2015. Developmental plasticity and evolution – quo vadis? Heredity, 115, 302–305.
Moran N A. 1992. The evolution of aphid life cycles. Annual Review of Entomology, 37, 321–348.
Nakane Y, Shimmura T, Abe H, Yoshimura T. 2014. Intrinsic photosensitivity of a deep brain photoreceptor. Current Biology, 24, R596–R597.
Normark B B, Moran N A. 2000. Testing for the accumulation of deleterious mutations in asexual eukaryote genomes using molecular sequence. Journal of Natural History, 34, 1719–1729.
Ogawa K, Miura T. 2014. Aphid polyphenisms: Trans-generational developmental regulation through viviparity. Frontiers in Physiology, 5, 1.
Oka Y, Kagami-Yashima C, Kagawa K, Sonoda S, Murai T. 2018. Clonal variation of sexual morph production in response to temperature and photoperiod in soybean aphid, Aphis glycines (Hemiptera: Aphididae). Applied Entomology and Zoology, 53, 509–517.
Ollivier M, Gabaldón T, Poulain J, Gavory F, Leterme N, Gauthier J P, Legeai F, Tagu D, Simon J C, Rispe C. 2012. Comparison of gene repertoires and patterns of evolutionary rates in eight aphid species that differ by reproductive mode. Genome Biology and Evolution, 4, 155–167.
Pearcy M, Aron S, Doums C, Keller L. 2004. Conditional use of sex and parthenogenesis for worker and queen production in ants. Science, 306, 1780–1783.
Peng X, Qiao X, Chen M. 2017. Responses of holocyclic and anholocyclic Rhopalosiphum padi populations to low-temperature and short-photoperiod induction. Ecology and Evolution, 7, 1030–1042.
Perotti M A, Young D K, Braig H R. 2016. The ghost sex-life of the paedogenetic beetle Micromalthus debilis. Scientific Reports, 6, 27364.
Poupoulidou D, Margaritopoulos J T, Kephalogianni T E, Zarpas K D, Tsitsipis J A. 2006. Effect of temperature and photoperiod on the life cycle in lineages of Myzus persicae nicotianae and Myzus persicae s.str. (Hemiptera: Aphididae). European Journal of Entomology, 103, 337–346.
Razmjou J, Vorburger C, Moharramipour S, Mirhoseini S Z, Fathipour Y. 2010. Host-associated differentiation and evidence for sexual reproduction in Iranian populations of the cotton aphid, Aphis gossypii. Entomologia Experimentalis et Applicata, 134, 191–199.
Riparbelli M G, Tagu D, Bonhomme J, Callaini G. 2005. Aster self-organization at meiosis: A conserved mechanism in insect parthenogenesis? Developmental Biology, 278, 220–230.
Rispe C, Bonhomme J, Simon J C. 1999. Extreme life-cycle and sex ratio variation among sexually produced clones of the aphid Rhopalosiphum padi (Homoptera: Aphididae). Oikos, 86, 254–264.
Rispe C, Pierre J S. 1998. Coexistence between cyclical parthenogens, obligate parthenogens, and intermediates in a fluctuating environment. Journal of Theoretical Biology, 195, 97–110.
Rispe C, Pierre J S, Gouyon P H. 1998. Models of sexual and asexual coexistence in aphids based on constraints. Journal of Evolutionary Biology, 11, 685–701.
Sabater-Muñoz B, Legeai F, Rispe C, Bonhomme J, Dearden P, Dossat C, Duclert A, Gauthier J P, Ducray D G, Hunter W, Dang P, Kambhampati S, Martinez-Torres D, Cortes T, Moya A, Nakabachi A, Philippe C, Prunier-Leterme N, Rahbé Y, Simon J C, et?al. 2006. Large scale gene discovery in the pea aphid Acyrthosiphon pisum (Hemiptera). Genome Biology, 7, R21.
Sandrock C, Razmjou J, Vorburger C. 2011. Climate effects on life cycle variation and population genetic architecture of the black bean aphid, Aphis fabae. Molecular Ecology, 20, 4165–4181.
Saunders D S. 1981. Insect photoperiodism - the clock and the count: A review. Physiological Entomology, 6, 99–116.
Shen D, Zhou F, Xu Z, He B, Li M, Shen J, Yin M, An C. 2014. Systemically interfering with immune response by a fluorescent cationic dendrimer delivered gene suppression. Journal of Materials Chemistry (B), 2, 4653–4659.
Simon J C, Martinez-Torres D, Latorre A, Moya A, Hebert P D N. 1996. Molecular characterization of cyclic and obligate parthenogens in the aphid Rhopalosiphum padi (L.). Proceedings of the Royal Society (B: Biological Sciences), 263, 481–486.
Simon J C, Rispe C, Sunnucks P. 2002. Ecology and evolution of sex in aphids. Trends in Ecology and Evolution, 17, 34–39.
Srinivasan D G, Abdelhady A, Stern D L. 2014. Gene expression analysis of parthenogenetic embryonic development of the pea aphid, Acyrthosiphon pisum, suggests that aphid parthenogenesis evolved from meiotic oogenesis. PLoS ONE, 9, e115099.
Steel C G H, Lees A D. 1977. The role of neurosecretion in the photoperiodic control of polymorphism in the aphid Megoura viciae. Journal of Experimental Biology, 67, 117–135.
Stunnikov V. 1975. Sex control in silkworms. Nature, 255, 111–113.
Sun Y, Guo H, Zhu-Salzman K, Ge F. 2013. Elevated CO2 increases the abundance of the peach aphid on Arabidopsis by reducing jasmonic acid defenses. Plant Science, 210, 128–140.
Sunnucks P, De Barro P J, Lushai G, Maclean N, Hales D. 1997. Genetic structure of an aphid studied using microsatellites: Cyclic parthenogenesis, differentiated lineages and host specialization. Molecular Ecology, 6, 1059–1073.
Tagu D, Sabater-Muñoz B, Simon J C. 2005. Deciphering reproductive polyphenism in aphids. Invertebrate Reproduction and Development, 48, 71–80.
Tanaka S. 2001. Endocrine mechanisms controlling body-color polymorphism in locusts. Archives of Insect Biochemistry and Physiology, 47, 139–149.
Le Trionnaire G, Hardie J, Jaubert-Possamai S, Simon J C, Tahu D. 2008. Shifting from clonal to sexual reproduction in aphids: physiological and developmental aspects. Biology of the Cell, 100, 441–451.
Le Trionnaire G, Jaubert S, Sabater-Muñoz B, Benedetto A, Bonhomme J, Prunier-Leterme N, Martinez-Torres D, Simon J C, Tagu D. 2007. Seasonal photoperiodism regulates the expression of cuticular and signaling protein genes in the pea aphid. Insect Biochemistry and Molecular Biology, 37, 1094–1102.
Uller T. 2008. Developmental plasticity and the evolution of parental effects. Trends in Ecology and Evolution, 23, 432–438.
Vorburger C, Sunnuck P, Ward S A. 2003. Explaining the coexistence of asexuals with their sexual progenitors: no evidence for general-purpose genotypes in obligate parthenogens of the peach potato aphid, Myzus persicae. Ecology Letters, 6, 1091–1098.
Westerlund S A, Hoffmann K H. 2004. Rapid quantification of juvenile hormones and their metabolites in insect haemolymph by liquid chromatography-mass spectrometry (LC-MS). Analytical and Bioanalytical Chemistry, 379, 540–543.
Wilson A C C, Sunnucks P, Hales D F. 1999. Microevolution, low clonal diversity and genetic affinities of parthenogenetic Sitobion aphids in New Zealand. Molecular Ecology, 8, 1655–1666.
Win K Y, Feng S S. 2005. Effects of particle size and surface coating on cellular uptake of polymeric nanoparticles for oral delivery of anticancer drugs. Biomaterials, 26, 2713–2722.
Xu A Y, Li M W, Sun P J, Zhang Y H, Hou C X. 2004. Review on silkworm (Bombyx mori) sex control in China. International Journal of Industrial Entomology, 8, 123–127.
Xu Z, He B, Wei W, Liu K, Yin M, Yang W, Shen J. 2014. Highly water-soluble perylenediimide-cored poly(amido amine) vector for efficient gene transfection. Journal of Materials Chemistry (B), 2, 3079–3086.
Xue B, Leibler S. 2018. Benefits of phenotypic plasticity for population growth in varying environments. Proceedings of the National Academy of Sciences of the United States of America, 115, 12745–12750.
Yan S, Li H T, Zhu W L, Zhu J L, Zhang Q W, Liu X X. 2014a. Effects of light intensity on the sexual behavior of the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae). Acta Entomologica Sinica, 57, 1045–1050. (in Chinese)
Yan S, Liu Y J, Zhang X F, Qin M, Liu H, Zhu J L, Li Z, Zhang Q W, Liu X X. 2017. Daily expression of Clock gene in compound eye of Helicoverpa armigera. Scientia Agricultura Sinica, 50, 3733–3744. (in Chinese)
Yan S, Liu Y J, Zhu J L, Cui W N, Zhang X F, Yang Y H, Liu X M, Zhang Q W, Liu X X. 2019. Daily expression of two circadian clock genes in compound eyes of Helicoverpa armigera: evidence for peripheral tissue circadian timing. Insect Science, 26, 217–228.
Yan S, Ni H, Li H, Zhang J, Liu X, Zhang Q. 2013. Molecular cloning, characterization, and mRNA expression of two cryptochrome genes in Helicoverpa armigera (Lepidoptera: Noctuidae). Journal of Economic Entomology, 106, 450–462.
Yan S, Qian J, Cai C, Ma Z, Li J, Yin M, Ren B, Shen J. 2020. Spray method application of transdermal dsRNA delivery system for efficient gene silencing and pest control on soybean aphid Aphis glycines. Journal of Pest Science, 93, 449–459.
Yan S, Zhu J, Zhu W, Zhang X, Li Z, Liu X, Zhang Q. 2014b. The expression of three opsin genes from the compound eyes of Helicoverpa armigera (Lepidoptera: Noctuidae) is regulated by a circadian clock, light conditions and nutritional status. PLoS ONE, 9, e11683.
Yashiro T, Matsuura K. 2014. Termite queens close the sperm gates of eggs switch from sexual to asexual reproduction. Proceedings of the National Academy of Sciences of the United States of America, 111, 17212–17217.
Yin M, Shen J, Gropeanu R, Pflugfelder G O, Weil T, Müllen K. 2008. Fluorescent core/shell nanoparticles for specific cell-nucleus staining. Small, 4, 894–898.
Yu N, Christiaens O, Liu J, Niu J, Cappelle K, Caccia S, Huvenne H, Smagghe G. 2013. Delivery of dsRNA for RNAi in insects: An overview and future directions. Insect Science, 20, 4–14.
Zera A J, Denno R F. 1997. Physiology and ecology of dispersal polymorphism in insects. Annual Review of Entomology, 42, 207–230.
Zhao H, Rossiter S J, Teeling E C, Li C, Cotton J A, Zhang S. 2009. The evolution of color vision in nocturnal mammals. Proceedings of the National Academy of Science of the United States of America, 106, 8980–8985.
Zheng Y, Hu Y, Yan S, Zhou H, Song D, Yin M, Shen J. 2019. A polymer/detergent formulation improves dsRNA penetration through the body wall and RNAi-induced mortality in the soybean aphid Aphis glycines. Pest Management Science, 75, 1993–1999.
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