Evolutionary mechanisms for camouflage in Cladomorphus phyllinus (Phasmatodea): A reflection on the role of evidence for hypotheses proposition

DIMITRI FORERO LUIZ ALEXANDRE CAMPOS VALENTINA CASTRO-HUERTAS FILIPE M. BIANCHI About the authors

Abstract

We address and discuss some of the many flaws exhibited by Costa et al. (2019)COSTA J, TORRES L, PROVANCE JR DW, BRUGNERA R & GRAZIA J. 2019. First report of predation by a stink bug (Supputius cincticeps Stål) on a walking-stick insect (Cladomorphus phyllinus Gray), with reflections on evolutionary mechanisms for camouflage. Acta Biol Par 48: 5-15. which tried to explain the twig-like camouflage of Cladomorphus phyllinus. Given the lack of both empirical and theoretical underpinnings in Costa et al. (2019)COSTA J, TORRES L, PROVANCE JR DW, BRUGNERA R & GRAZIA J. 2019. First report of predation by a stink bug (Supputius cincticeps Stål) on a walking-stick insect (Cladomorphus phyllinus Gray), with reflections on evolutionary mechanisms for camouflage. Acta Biol Par 48: 5-15., we call into question the validity of their conclusions, in particular, that horizontal gene transfer is a causal mechanism for the camouflage in C. phyllinus.

Key words
Hemiptera; lateral gene transfer; stink bug; walking-stick insect

INTRODUCTION

“Extraordinary claims require extraordinary evidence.” ― Carl Sagan

In a recent paper, Costa et al. (2019)COSTA J, TORRES L, PROVANCE JR DW, BRUGNERA R & GRAZIA J. 2019. First report of predation by a stink bug (Supputius cincticeps Stål) on a walking-stick insect (Cladomorphus phyllinus Gray), with reflections on evolutionary mechanisms for camouflage. Acta Biol Par 48: 5-15. [from now on CEA] offer a report on the predation of a species of predatory stink bug [Supputius cincticeps (Stål, 1860) (Hemiptera, Pentatomidae, Asopinae)] over a walking-stick insect [Cladomorphus phyllinus Gray, 1835 (Phasmatodea, Phasmatidae, Cladomorphinae)]. The paper presents natural history observations on this interaction but further proposes an astonishing claim: that the twig aspect of this species of Phasmatodea could have arisen through horizontal gene transfer (HGT) of a morph plant gene via the stink bug. Given that very little is known about the mechanisms of morphogenesis in animals, and in insects in particular, any hypothesis of evolutionary camouflage mechanism in walking-stick insects invoking a morphogene should be adequately substantiated. Here, we present some arguments that doubt the validity of CEA statements and strongly reject the notion of these statements being scientific hypotheses.

DISCUSSION

In their paper, CEA claimed that their observations are the first report of predation between Asopinae over Phasmatodea; nonetheless records of predator-prey interaction between Asopinae and Phasmatodea go back more than a century (e.g., Kirkland 1898KIRKLAND AH. 1898. The species of Podisus occurring in the United States. Rept Mass St Bd. Agr 45: 412-439, Appendix: 112-138.), and interactions between Asopinae species and their prey are opportunistic (de Clercq 2000DE CLERCQ P. 2000. Predaceous Stinkbugs (Pentatomidae: Asopinae). In: Schaefer CW & Panizzi AR (Eds), Heteroptera of Economic Importance, Boca Raton: CRC Press, Florida, USA, p. 759-812.). The interaction documented by CEA thus seems to be casual and uncommon given that it was carried out under laboratory conditions and based on a single observation of a S. cincticeps nymph.

The core of CEA paper presented an alternative idea on how camouflage could have evolved in Phasmatodea, different from the evolution of masquerade camouflage (Skelhorn et al. 2010SKELHORN J, ROWLAND HM, SPEED MP & RUXTON GD. 2010. Masquerade: Camouflage Without Crypsis. Science 327(5691): 51., Dias Lima & Kaminski 2019DIAS LIMA L & KAMINSKI LA. 2019. Camouflage. In: Vonk J & Shackelford T (Eds), Encyclopedia of Animal Cognition and Behavior, Springer, Cham, Switzerland, p. 1-9.). The authors weave assumptions related to zoophytophagy, HGT, and camouflage to speculate a causality link between the predation of S. cinctipes over C. phyllinus, and the particular phenotype of this species of Phasmatodea. With such a great claim, the reader could expect a careful exposition of theories and correct use of methods and techniques designed to explore in-depth the morphological, behavioral, and molecular data involved in this predator-prey system (e.g., Lin et al. 2016LIN X, FARIDI N & CASOLA C. 2016. An ancient transkingdom horizontal transfer of Penelope-like retroelements from arthropods to conifers. Genome Biol Evol 8(4): 1252-1266., Gao et al. 2018GAO D, CHU Y, XIA H, XU C, HEYDUK K, ABERNATHY B, OZIAS-AKINS P, LEEBENSMACK JH & JACKSON SA. 2018. Horizontal transfer of non-LTR retrotransposons from arthropods to flowering plants, Mol Biol Evol 35(2): 354-364.). Unfortunately, this was not the case. Instead, CEA relied on non-supported ideas to substantiate their unusual claim. CEA invoked HGT from a plant species to a Phasmatodea via a Pentatomidae predator with nonexclusive phytophagous habit. This argumentation gravely suffers from various issues. The first is that they argue that S. cinctipes need to feed on plants to complete its life-cycle. Nonetheless, the results of experimental research using only animal prey (e.g., Tenebrio molitor L., Musca domestica L.), comparing longevity, fertility, and other biological parameters (e.g., Beserra et al. 1995BESERRA EB, ZANUNCIO TV, ZANUNCIO JC & SANTOS GP. 1995. Desenvolvimento de Supputius cincticeps (Heteroptera, Pentatomidae) alimentado com larvas de Zophobas confusa, Tenebrio molitor (Coleoptera, Tenebrionidae) e Musca domestica (Diptera, Muscidae). Rev Bras Zool 12: 725-733., Zanuncio et al. 1997ZANUNCIO JC, TORRES JB, BERNARDO DL & DE CLERCQ PD. 1997. Effects of prey switching on nymphal development of four species of predatory stink bugs. Mededelingen Faculteit Landbouwkundige en Toegepaste Biologische Wetenschappen Universiteit Gent (Belgium) 62(2): 483-490., 2005, Oliveira et al. 2003OLIVEIRA I, ZANUNCIO JC, SERRÃO JE & PEREIRA JMM. 2003. Reproductive potential of the predator Supputius cincticeps (Heteroptera: Pentatomidae) affected by female body weight. Acta Sci Biol Sci 25: 49-53.) do not support this claim. Supputius cincticeps is indeed a generalist predator that may have an advantage in longevity when supplementing their diet with plant tissue (Zanuncio et al. 2004ZANUNCIO JC, LACERDA MC, ZANUNCIO JUNIOR JS, ZANUNCIO TV, SILVA AMC & ESPINDULA MC. 2004. Fertility table and rate of population growth of the predator Supputius cincticeps (Heteroptera: Pentatomidae) on one plant of Eucalyptus cloeziana in the field. Ann appl Biol 144: 357-361.), although plant feeding is not necessary for its development. Furthermore, S. cinctipes, as well as all other asopines, are predatory species that cause the death of their prey during its feeding (Martínez et al. 2016MARTÍNEZ LC, FIALHO MDCQ, BARBOSA LCA, OLIVEIRA LL, ZANUNCIO JC & SERRÃO JE. 2016. Stink bug predator kills prey with salivary non-proteinaceous compounds. Insect Biochem Mol Biol 68: 71-78., Walker et al. 2016WALKER AA, WEIRAUCH C, FRY BG & KING GF. 2016. Venoms of heteropteran insects: a treasure trove of diverse pharmacological toolkits. Toxins 8(2): 1-32.), not fulfilling the goal of HGT process, which is the transfer of genetic material to another non-related organism and inserting these elements permanently. Therefore, the probability of S. cinctipes being a vector responsible for any HGT is very low.

HGT is the acquisition of genes from organisms other than a direct ancestor (Crisp et al. 2015CRISP A, BOSCHETTI C, PERRY M, TUNNACLIFFE A & MICKLEM G. 2015. Expression of multiple horizontally acquired genes is a hallmark of both vertebrate and invertebrate genomes. Genome Biol 16(1): 50.). These transfers are common within Bacteria, Archaea, and between them (e.g., Ochman et al. 2000OCHMAN H, LAWRENCE JG & GROLSMAN EA. 2000 Lateral gene transfer and the nature of bacterial innovation. Nature 405: 299-304., Gophna et al. 2004GOPHNA U, CHARLEBOIS RL & DOOLITTLE WF. 2004. Have archaeal genes contributed to bacterial virulence? Trends Microbiol 12: 213-219.). HGT involving Eukarya is more uncommon than compared to prokaryotes (Syvanen 2012SYVANEN M. 2012. Evolutionary implications of horizontal gene transfer. Annu Rev Genet 46: 341-358.). Although it is a highly complex process, given that the transmitted genes must be introduced in germline cells (Blaxter 2007BLAXTER M. 2007. Symbiont genes in host genomes: fragments with a future? Cell Host Microbe 2: 211-213.), successful HGT cases have been documented in Animalia (e.g., Moran & Jarvik 2010MORAN NA & JARVIK T. 2010. Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 328(5978): 624-627., Walsh et al. 2013WALSH AM, KORTSCHAK RD, GARDNER MG, BERTOZZI T & ADELSON DL. 2013. Widespread horizontal transfer of retrotransposons. PNAS 110(3): 1012-1016.), Plantae (e.g., Baidouri et al. 2014BAIDOURI MEL ET AL. 2014. Widespread and frequent horizontal transfers of transposable elements in plants. Genome Res 24(5): 831-838.), and Fungi (e.g., Novikova et al. 2010NOVIKOVA O, SMYSHLYAEV G & BLINOV A. 2010. Evolutionary genomics revealed interkingdom distribution of Tcn1-like chromodomain-containing Gypsy LTR retrotransposons among fungi and plants. BMC Genomics 11(1): 231.). However, even genes successfully transmitted and integrated into an organism are not necessarily transcribed in the recipient cell (Nikoh et al. 2008NIKOH N, TANAKA K, SHIBATA F, KONDO N, HIZUME M, SHIMADA M & FUKATSU T. 2008. Wolbachia genome integrated in an insect chromosome: evolution and fate of laterally transferred endosymbiont genes. Genome Res 18(2): 272-280.). A few instances of HGT involving retroelements of plants and arthropods are known, involving genomic elements from arthropods to spermatophytes (Lin et al. 2016LIN X, FARIDI N & CASOLA C. 2016. An ancient transkingdom horizontal transfer of Penelope-like retroelements from arthropods to conifers. Genome Biol Evol 8(4): 1252-1266., Gao et al. 2018GAO D, CHU Y, XIA H, XU C, HEYDUK K, ABERNATHY B, OZIAS-AKINS P, LEEBENSMACK JH & JACKSON SA. 2018. Horizontal transfer of non-LTR retrotransposons from arthropods to flowering plants, Mol Biol Evol 35(2): 354-364.), as well as from plants or fungi into arthropods (e.g., Moran & Jarvik 2010MORAN NA & JARVIK T. 2010. Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 328(5978): 624-627., Altincicek et al. 2012ALTINCICEK B, KOVACS JL & GERARDO NM. 2012. Horizontally transferred fungal carotenoid genes in the two-spotted spider mite Tetranychus urticae. Biol Letters 8(2): 253-257., Zakharov 2016ZAKHAROV IA. 2016. Horizontal gene transfer into the genomes of insects. Russ J Genet 52: 702-707.). In all instances of HGT involving arthropods, there is no consensus as to how the process was achieved (e.g., Wybouw et al. 2012WYBOUW N, BALABANIDOU V, BALLHORN DJ, DERMAUW W, GRBIĆ M, VONTAS J & VAN LEEUWEN T. 2012. A horizontally transferred cyanase gene in the spider mite Tetranychus urticae is involved in cyanate metabolism and is differentially expressed upon host plant change. Insect Biochem Mol Biol 42: 881-889.), but always involved genes only with particular metabolic functions (Grbić et al. 2011GRBIĆ M ET AL. 2011. The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 479(7374): 487-492., Wybouw et al. 2012WYBOUW N, BALABANIDOU V, BALLHORN DJ, DERMAUW W, GRBIĆ M, VONTAS J & VAN LEEUWEN T. 2012. A horizontally transferred cyanase gene in the spider mite Tetranychus urticae is involved in cyanate metabolism and is differentially expressed upon host plant change. Insect Biochem Mol Biol 42: 881-889., Nováková & Moran 2012NOVÁKOVÁ E & MORAN NA. 2012. Diversification of Genes for Carotenoid Biosynthesis in Aphids following an Ancient Transfer from a Fungus. Mol Biol Evol 29: 313-323.). Thus, it is assumed that HGT in arthropods will correspond to very specific gene functions.

The most critical and flawed argument of CEA paper is that the camouflage exhibited by C. phyllinus is the result of HGT “of plant-derived genetic material leading to development of a form resembling a tree stem”. This assumption is highly problematic in several respects. First, very little is known about the control of plant morphology. A fundamental question in plant biology is how different plant phenotypes arise based on particular genetic information, and how the environment interacts with this information to produce distinct phenotypes. Although this question is just starting to be answered (e.g., Schlichting & Pigliucci 1993SCHLICHTING CD & PIGLIUCCI M. 1993. Control of phenotypic plasticity via regulatory genes. Amer Naturalist 142: 366-370., Yang et al. 2014YANG W ET AL. 2014. Combining high-throughput phenotyping and genome-wide association studies to reveal natural genetic variation in rice. Nat Commun 8(5): 5087., Casacuberta et al. 2016CASACUBERTA JM, JACKSON S, PANAUD O, PURUGGANAN M & WENDEL J. 2016. Evolution of plant phenotypes, from genomes to traits. G3: Genes, Genomes, Genetics 6: 775-778., Gaudinier & Brady 2016GAUDINIER A & BRADY SM. 2016. Mapping Transcriptional Networks in Plants: DataDriven Discovery of Novel Biological Mechanisms. Annu Rev Plant Biol 67: 575-594., Honkanen et al. 2016HONKANEN ET AL. 2016. The mechanism forming the cell surface of tip-growing rooting cells is conserved among land plants. Curr Biol 26: 3238-3244.), it is clear, as recent research suggests, that plant phenotypes are the result of polygenic control (Ogura & Busch 2016OGURA T & BUSCH W. 2016. Genotypes, networks, phenotypes: moving toward plant systems genetics. Annu Rev Cell Dev Biol 32: 103-126., Bucksch et al. 2017BUCKSCH A ET AL. 2017. Morphological Plant Modeling: Unleashing Geometric and Topological Potential within the Plant Sciences. Front Plant Sci 8: 900.), and thus must be assumed that several loci are responsible in producing particular phenotypes on specific parts of plants. CEA did not provide a plausible explanation as to how all these genetic elements were transferred and inserted into the insect. This is also highly problematic because they failed to provide a theoretical underpinning that might help explain how the whole suite of genes involved in plant morphogenesis might adequately function in another organism with radically different genetic control mechanisms. Thus, the failure is twofold, lacking both empirical evidence and theoretical support that might allow other researchers to test these ideas.

Finally, CEA implicitly expand the HGT process to other Phasmatodea, wrongly assuming that all species in the order are twig-like, which is not the case. Phasmatodea exhibit various body types, resembling various plant forms such as twigs, leaves, or moss (Bradler & Buckley 2020BRADLER S & BUCKLEY TR. 2020. Biodiversity of Phasmatodea. In: Foottit RG & Adler PH (Eds), Insect Biodiversity: Science and Society, Hoboken: John Wiley & Sons, New Jersey, USA, p. 281-313.), and thus are probably the result of various evolutionary selective pressures, as evidenced by the various phylogenetic patterns recovered (Whiting et al. 2003WHITING M, BRADLER S & MAXWELL T. 2003. Loss and recovery of wings in stick insects. Nature 421: 264-267., Bradler et al. 2014BRADLER S, ROBERTSON JA & WHITING MF. 2014. A molecular phylogeny of Phasmatodea with emphasis on Necrosciinae, the most species-rich subfamily of stick insects. Syst Entomol 39: 205-222., Robertson et al. 2018ROBERTSON JA, BRADLER S & WHITING MF. 2018. Evolution of oviposition techniques in stick and leaf insects (Phasmatodea). Front Ecol Evol 6: 216.). If HGT is responsible for the twig-like appearance of C. phyllinus, then it should have been explained how other species of Phasmatodea also present similar plant-looking body types, another idea that was never properly discussed in their paper.

CONCLUSIONS

A single observation of S. cinctipes feeding to C. phyllinus, lacking additional empirical and theoretical support, prevents to postulate HGT as the driving mechanism explaining the camouflage in this phasmatodean species. In a broad sense, scientific evidence is something that gives a scientist a good reason to consider a hypothesis true (Achinstein 2008ACHINSTEIN P. 2008. Evidence. In: Psillos S & Curd M (Eds), The Routledge companion to philosophy of science. London: Routledge, p. 337-348.), being this evidence filtered through a personal judgment and then interpreted as strong, weak, incomplete, redundant, inconclusive, plausible, and so on (Schum 2001SCHUM DA. 2001. The evidential foundations of probabilistic reasoning. Evanston: Northwestern University Press, 545 p.). Scientific evidence gains its value not from using empirical data alone, but from how the evidence was produced, and to which theories the conclusions based on this evidence are compared to (Bogen 2017BOGEN J. 2017. Theory and observation in science. In: The Stanford Encyclopedia of Philosophy (Summer 2017 Edition), Zalta EN (Ed), Available at: https://plato.stanford.edu/archives/sum2017/entries/science-theory-observation/.
https://plato.stanford.edu/archives/sum2...
). The zenith of evolutionary biology is the building of narratives based on evidence. However, the mere concatenation of evidence in a coherent sequence attributing causality between them is not subject to confirmation or disconfirmation (Abbott 1992ABBOTT A. 1992. From causes to events. Notes on narrative positivism. Sociol Method Res 20: 428-455., Mink 1987MINK LO. 1987. Narrative form as a cognitive instrument. In: Fay B, Golub EO & Vann RT (Eds), Historical understanding, Ithaca: Cornell University Press, New York, USA, p. 182-203.). Regrettably, CEA paper lacks both empirical data and theoretical postulates to properly advance a scientific theory with regard to Phasmatodea camouflage. Finally, all this argumentation calls for a stronger peer-review process of our ideas submitted to scientific journals, in order to produce better science.

REFERENCES

  • ABBOTT A. 1992. From causes to events. Notes on narrative positivism. Sociol Method Res 20: 428-455.
  • ACHINSTEIN P. 2008. Evidence. In: Psillos S & Curd M (Eds), The Routledge companion to philosophy of science. London: Routledge, p. 337-348.
  • ALTINCICEK B, KOVACS JL & GERARDO NM. 2012. Horizontally transferred fungal carotenoid genes in the two-spotted spider mite Tetranychus urticae. Biol Letters 8(2): 253-257.
  • BAIDOURI MEL ET AL. 2014. Widespread and frequent horizontal transfers of transposable elements in plants. Genome Res 24(5): 831-838.
  • BESERRA EB, ZANUNCIO TV, ZANUNCIO JC & SANTOS GP. 1995. Desenvolvimento de Supputius cincticeps (Heteroptera, Pentatomidae) alimentado com larvas de Zophobas confusa, Tenebrio molitor (Coleoptera, Tenebrionidae) e Musca domestica (Diptera, Muscidae). Rev Bras Zool 12: 725-733.
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    » https://plato.stanford.edu/archives/sum2017/entries/science-theory-observation/
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  • BRADLER S, ROBERTSON JA & WHITING MF. 2014. A molecular phylogeny of Phasmatodea with emphasis on Necrosciinae, the most species-rich subfamily of stick insects. Syst Entomol 39: 205-222.
  • BUCKSCH A ET AL. 2017. Morphological Plant Modeling: Unleashing Geometric and Topological Potential within the Plant Sciences. Front Plant Sci 8: 900.
  • CASACUBERTA JM, JACKSON S, PANAUD O, PURUGGANAN M & WENDEL J. 2016. Evolution of plant phenotypes, from genomes to traits. G3: Genes, Genomes, Genetics 6: 775-778.
  • COSTA J, TORRES L, PROVANCE JR DW, BRUGNERA R & GRAZIA J. 2019. First report of predation by a stink bug (Supputius cincticeps Stål) on a walking-stick insect (Cladomorphus phyllinus Gray), with reflections on evolutionary mechanisms for camouflage. Acta Biol Par 48: 5-15.
  • CRISP A, BOSCHETTI C, PERRY M, TUNNACLIFFE A & MICKLEM G. 2015. Expression of multiple horizontally acquired genes is a hallmark of both vertebrate and invertebrate genomes. Genome Biol 16(1): 50.
  • DE CLERCQ P. 2000. Predaceous Stinkbugs (Pentatomidae: Asopinae). In: Schaefer CW & Panizzi AR (Eds), Heteroptera of Economic Importance, Boca Raton: CRC Press, Florida, USA, p. 759-812.
  • DIAS LIMA L & KAMINSKI LA. 2019. Camouflage. In: Vonk J & Shackelford T (Eds), Encyclopedia of Animal Cognition and Behavior, Springer, Cham, Switzerland, p. 1-9.
  • GAO D, CHU Y, XIA H, XU C, HEYDUK K, ABERNATHY B, OZIAS-AKINS P, LEEBENSMACK JH & JACKSON SA. 2018. Horizontal transfer of non-LTR retrotransposons from arthropods to flowering plants, Mol Biol Evol 35(2): 354-364.
  • GAUDINIER A & BRADY SM. 2016. Mapping Transcriptional Networks in Plants: DataDriven Discovery of Novel Biological Mechanisms. Annu Rev Plant Biol 67: 575-594.
  • GOPHNA U, CHARLEBOIS RL & DOOLITTLE WF. 2004. Have archaeal genes contributed to bacterial virulence? Trends Microbiol 12: 213-219.
  • GRBIĆ M ET AL. 2011. The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 479(7374): 487-492.
  • HONKANEN ET AL. 2016. The mechanism forming the cell surface of tip-growing rooting cells is conserved among land plants. Curr Biol 26: 3238-3244.
  • KIRKLAND AH. 1898. The species of Podisus occurring in the United States. Rept Mass St Bd. Agr 45: 412-439, Appendix: 112-138.
  • LIN X, FARIDI N & CASOLA C. 2016. An ancient transkingdom horizontal transfer of Penelope-like retroelements from arthropods to conifers. Genome Biol Evol 8(4): 1252-1266.
  • MARTÍNEZ LC, FIALHO MDCQ, BARBOSA LCA, OLIVEIRA LL, ZANUNCIO JC & SERRÃO JE. 2016. Stink bug predator kills prey with salivary non-proteinaceous compounds. Insect Biochem Mol Biol 68: 71-78.
  • MINK LO. 1987. Narrative form as a cognitive instrument. In: Fay B, Golub EO & Vann RT (Eds), Historical understanding, Ithaca: Cornell University Press, New York, USA, p. 182-203.
  • MORAN NA & JARVIK T. 2010. Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 328(5978): 624-627.
  • NIKOH N, TANAKA K, SHIBATA F, KONDO N, HIZUME M, SHIMADA M & FUKATSU T. 2008. Wolbachia genome integrated in an insect chromosome: evolution and fate of laterally transferred endosymbiont genes. Genome Res 18(2): 272-280.
  • NOVÁKOVÁ E & MORAN NA. 2012. Diversification of Genes for Carotenoid Biosynthesis in Aphids following an Ancient Transfer from a Fungus. Mol Biol Evol 29: 313-323.
  • NOVIKOVA O, SMYSHLYAEV G & BLINOV A. 2010. Evolutionary genomics revealed interkingdom distribution of Tcn1-like chromodomain-containing Gypsy LTR retrotransposons among fungi and plants. BMC Genomics 11(1): 231.
  • OCHMAN H, LAWRENCE JG & GROLSMAN EA. 2000 Lateral gene transfer and the nature of bacterial innovation. Nature 405: 299-304.
  • OGURA T & BUSCH W. 2016. Genotypes, networks, phenotypes: moving toward plant systems genetics. Annu Rev Cell Dev Biol 32: 103-126.
  • OLIVEIRA I, ZANUNCIO JC, SERRÃO JE & PEREIRA JMM. 2003. Reproductive potential of the predator Supputius cincticeps (Heteroptera: Pentatomidae) affected by female body weight. Acta Sci Biol Sci 25: 49-53.
  • ROBERTSON JA, BRADLER S & WHITING MF. 2018. Evolution of oviposition techniques in stick and leaf insects (Phasmatodea). Front Ecol Evol 6: 216.
  • SCHUM DA. 2001. The evidential foundations of probabilistic reasoning. Evanston: Northwestern University Press, 545 p.
  • SCHLICHTING CD & PIGLIUCCI M. 1993. Control of phenotypic plasticity via regulatory genes. Amer Naturalist 142: 366-370.
  • SKELHORN J, ROWLAND HM, SPEED MP & RUXTON GD. 2010. Masquerade: Camouflage Without Crypsis. Science 327(5691): 51.
  • SYVANEN M. 2012. Evolutionary implications of horizontal gene transfer. Annu Rev Genet 46: 341-358.
  • WALKER AA, WEIRAUCH C, FRY BG & KING GF. 2016. Venoms of heteropteran insects: a treasure trove of diverse pharmacological toolkits. Toxins 8(2): 1-32.
  • WALSH AM, KORTSCHAK RD, GARDNER MG, BERTOZZI T & ADELSON DL. 2013. Widespread horizontal transfer of retrotransposons. PNAS 110(3): 1012-1016.
  • WHITING M, BRADLER S & MAXWELL T. 2003. Loss and recovery of wings in stick insects. Nature 421: 264-267.
  • WYBOUW N, BALABANIDOU V, BALLHORN DJ, DERMAUW W, GRBIĆ M, VONTAS J & VAN LEEUWEN T. 2012. A horizontally transferred cyanase gene in the spider mite Tetranychus urticae is involved in cyanate metabolism and is differentially expressed upon host plant change. Insect Biochem Mol Biol 42: 881-889.
  • YANG W ET AL. 2014. Combining high-throughput phenotyping and genome-wide association studies to reveal natural genetic variation in rice. Nat Commun 8(5): 5087.
  • ZAKHAROV IA. 2016. Horizontal gene transfer into the genomes of insects. Russ J Genet 52: 702-707.
  • ZANUNCIO JC, LACERDA MC, ZANUNCIO JUNIOR JS, ZANUNCIO TV, SILVA AMC & ESPINDULA MC. 2004. Fertility table and rate of population growth of the predator Supputius cincticeps (Heteroptera: Pentatomidae) on one plant of Eucalyptus cloeziana in the field. Ann appl Biol 144: 357-361.
  • ZANUNCIO JC, TORRES JB, BERNARDO DL & DE CLERCQ PD. 1997. Effects of prey switching on nymphal development of four species of predatory stink bugs. Mededelingen Faculteit Landbouwkundige en Toegepaste Biologische Wetenschappen Universiteit Gent (Belgium) 62(2): 483-490.
  • ZANUNCIO JC, BESERRA EB, MOLINA-RUGAMA AJ, ZANUNCIO TV, PINON TBM & MAFFIA VP. 2005. Reproduction and longevity of Supputius cincticeps (Het.: Pentatomidae) fed with larvae of Zophobas confusa, Tenebrio molitor (Col.: Tenebrionidae) or Musca domestica (Dip.: Muscidae). Braz Arch Biol Technol 48(5): 771-777.

Publication Dates

  • Publication in this collection
    13 July 2020
  • Date of issue
    2020

History

  • Received
    14 Feb 2020
  • Accepted
    20 Mar 2020
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