Abstract
We identified the antifungal gene termicin in three species of Cryptocercus woodroaches. Cryptocercus represents the closest living cockroach lineage of termites, which suggests that the antifungal role of termicin evolved prior to the divergence of termites from other cockroaches. An analysis of Cryptocercus termicin and two β-1,3-glucanase genes (GNBP1 and GNBP2), which appear to work synergistically with termicin in termites, revealed evidence of selection in these proteins. We identified the signature of past selective sweeps within GNBP2 from Cryptocercus punctulatus and Cryptocercus wrighti. The signature of past selective sweeps was also found within termicin from Cryptocercus punctulatus and Cryptocercus darwini. Our analysis further suggests a phenotypically identical variant of GNBP2 was maintained within Cryptocercus punctulatus, Cryptocercus wrighti, and Cryptocercus darwini while synonymous sites diverged. Cryptocercus termicin and GNBP2 appear to have experienced similar selective pressure to that of their termite orthologues in Reticulitermes. This selective pressure may be a result of ubiquitous entomopathogenic fungal pathogens such as Metarhizium. This study further reveals the similarities between Cryptocercus woodroaches and termites.
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References
Aldrich B, Krafsur E, Kambhampati S (2004) Species-specific allozyme markers for Appalachian wood-feeding cockroaches (Dictyoptera: Cryptocercidae). Biochem Genet 42(5):149–164
Bell WJ, Roth LM, Nalepa CA (2007) Cockroaches: ecology, behavior, and natural history. Johns Hopkins University Press, Baltimore
Bulmer MS, Crozier RH (2004) Duplication and diversifying selection among termite antifungal peptides. Mol Biol Evol 21(12):2256–2264
Bulmer MS, Crozier RH (2006) Variation in positive selection in termite GNBPs and Relish. Mol Biol Evol 23(2):317–326
Bulmer MS, Bachelet I, Raman R, Rosengaus RB, Sasisekharan R (2009) Targeting an antimicrobial effector function in insect immunity as a pest control strategy. Proc Natl Acad Sci USA 106(31):12652–12657
Bulmer MS, Lay F, Hamilton C (2010) Adaptive evolution in subterranean termite antifungal peptides. Insect Mol Biol 19(5):669–674
Bulmer MS, Denier D, Velenovsky J, Hamilton C (2012) A common antifungal defense strategy in Cryptocercus woodroaches and termites. Insectes Soc 59:469–478
Burnside CA, Smith PT, Kambhampati S (1999) Three new species of the wood roach, Cryptocercus (Blattodea: Cryptocercidae), from the eastern United States. J Kans Entomol Soc 72:361–378
Da Silva P, Jouvensal L, Lamberty M, Bulet P, Caille A, Vovelle F (2003) Solution structure of termicin, an antimicrobial peptide from the termite Pseudacanthotermes spiniger. Protein Sci 12(3):438–446
Denier D, Bulmer MS (2015) Variation in subterranean termite susceptibility to fatal infections by local Metarhizium soil isolates. Insectes Soc 62(2):219–226. doi:10.1007/s00040-015-0394-6
Engel MS, Grimaldi DA, Krishna K (2009) Termites (Isoptera): their phylogeny, classification, and rise to ecological dominance. Am Mus Novit 3650:1–27
Gillespie JP, Bailey AM, Cobb B, Vilcinskas A (2000) Fungi as elicitors of insect immune responses. Arch Insect Biochem Physiol 44(2):49–68
Hamilton C, Bulmer MS (2012) Molecular antifungal defenses in subterranean termites: RNA interference reveals in vivo roles of termicins and GNBPs against a naturally encountered pathogen. Dev Comp Immunol 36:372–377
Hamilton C, Lay F, Bulmer MS (2011) Subterranean termite prophylactic secretions and external antifungal defenses. J Insect Physiol 57:1259–1266
Hegedüs N, Marx F (2013) Antifungal proteins: more than antimicrobials? Fungal Biol Rev 26(4):132–145. doi:10.1016/j.fbr.2012.07.002
Hossain S, Kambhampati S (2001) Phylogeny of Cryptocercus species (Blattodea: Cryptocercidae) inferred from nuclear ribosomal DNA. Mol Phylogenet Evol 21(1):162–165
Inward D, Beccaloni G, Eggleton P (2007) Death of an order: a comprehensive molecular phylogenetic study confirms that termites are eusocial cockroaches. Biol Lett 3(3):331–335
Janeway CA, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20:197–216
Korb J, Poulsen M, Hu H, Li C, Boomsma J, Zhang G, Liebig J (2015) A genomic comparison of two termites with different social complexity. Frontiers in Genetics. doi:10.3389/fgene.2015.00009
Krishna K, Grimaldi D, Krishna V, Engel M (2013) Treatise on the Isoptera of the World. Bull Am Mus Nat History B377(1):973–1495
Lamberty M, Zachary D, Lanot R, Bordereau C, Robert A, Hoffmann JA, Bulet P (2001) Insect immunity constitutive expression of a cysteine-rich antifungal and a linear antibacterial peptide in a termite insect. J Biol Chem 276(6):4085–4092
Lo N, Tokuda G, Watanabe H, Rose H, Slaytor M, Maekawa K, Bandi C, Noda H (2000) Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches. Curr Biol 10(13):801–804
McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351(6328):652–654
Milner RJ, Staples JA, Hartley TR, Lutton GG, Driver F, Watson JAL (1998) Occurrence of Metarhizium anisopliae in nests and feeding sites of Australian termites. Mycological Research 102:216–220
Nalepa CA (1984) Colony composition, protozoan transfer and some life history characteristics of the woodroach Cryptocercus punctulatus Scudder (Dictyoptera: Cryptocercidae). Behav Ecol Sociobiol 14(4):273–279
Nalepa CA (1988) Cost of parental care in the woodroach Cryptocercus punctulatus Scudder (Dictyoptera: Cryptocercidae). Behav Ecol Sociobiol 23(3):135–140
Nalepa CA (2005) Cryptocercus punctulatus (Dictyoptera: Cryptoceridae): dispersal evenst associated with rainfall. Entomol Mon Mag 141:95–97
Nalepa C (2010) Altricial development in subsocial cockroach ancestors: foundation for the evolution of phenotypic plasticity in termites. Evolut Dev 12(1):95–105
Nalepa CA (2011a) Altricial development in wood-feeding cockroaches: the key antecedent of termite eusociality. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, London, pp 69–95
Nalepa CA (2011b) Body size and termite evolution. Evol Biol 38:243–257. doi:10.1007/s11692-011-9121-z
Ohkuma M, Noda S, Hongoh Y, Nalepa CA, Inoue T (2009) Inheritance and diversification of symbiotic trichonymphid flagellates from a common ancestor of termites and the cockroach Cryptocercus. Proc R Soc Lond B 276(1655):239–245
Rambaut A (2002) Sequence Alignment Editor. Department of Zoology, University of Oxford, Oxford. http://evolve.zoo.ox.ac.uk
Roberts DW, Humber RA (1981) Entomogenous fungi. In: Cole GT, Kendrick B (eds) Biology of conidial fungi, vol 2. Academic Press, New York, pp 201–236
Roberts DW, St Leger RJ (2004) Metarhizium spp., cosmopolitan insect-pathogenic fungi: mycological aspects. Adv Appl Microbiol 54:1–70
Rosengaus RB, Traniello JFA, Bulmer MS (2011) Ecology, behavior and evolution of disease resistance in termites. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, London, pp 165–192
Rozas J, Rozas R (1999) DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15(2):174
Schmid-Hempel P (1998) Parasites in social insects. Monographs in behavior and ecology. Princeton University Press, Princeton
Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105(2):437
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3):585–595
Terrapon N, Li C, Robertson H, Ji L, Meng X, Booth W, Chen Z, Childers C, Glastad K, Gokhale K, Gowin J, Gronenberg W, Hermansen RA, Hu H, Hunt BG, Huylmans AK, Khalil SMS, Mitchell RD, Munoz-Torres MC, Mustard JA, Pan H, Reese JT, Scharf ME, Sun F, Vogel H, Xiao J, Yang W, Yang Z, Yang Z, Zhou J, Zhu J, Brent CS, Elsik CG, Goodisman MAD, Liberles DA, Roe RM, Vargo EL, Vilcinskas A, Wang J, Bornberg-Bauer E, Korb J, Zhang G, Liebig Jr (2014) Molecular traces of alternative social organization in a termite genome. Nat Commun. doi:10.1038/ncomms4636
Unckless RL, Lazzaro BP (2016) The potential for adaptive maintenance of diversity in insect antimicrobial peptides. Philos Trans R Soc Lond Ser B Biol Sci 371(1695):20150291
Vey A, Matha V, Dumas C (2002) Effects of the peptide mycotoxin destruxin E on insect haemocytes and on dynamics and efficiency of the multicellular immune reaction. J Invert Pathol 80(3):177–187
Wang C, St Leger RJ (2006) A collagenous protective coat enables Metarhizium anisopliae to evade insect immune responses. Proc Natl Acad Sci USA 103(17):6647–6652
Ye W, Lee C, Scheffrahn R, Aleong J, Su N, Bennett G, Scharf M (2004) Phylogenetic relationships of nearctic Reticulitermes species (Isoptera: Rhinotermitidae) with particular reference to Reticulitermes arenincola Goellner. Mol Phylogenet Evol 30(3):815–822
Zoberi MH (1995) Metarhizium anisopliae, a fungal pathogen of Reticulitermes flavipes (Isoptera: Rhinotermitidae). Mycologia 87(3):354–359
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Velenovsky, J.F., Kalisch, J. & Bulmer, M.S. Selective sweeps in Cryptocercus woodroach antifungal proteins. Genetica 144, 547–552 (2016). https://doi.org/10.1007/s10709-016-9923-0
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DOI: https://doi.org/10.1007/s10709-016-9923-0