Parasitology Research

, Volume 116, Issue 1, pp 237–242 | Cite as

Discrimination between lineage-specific shelters by bat- and human-associated bed bugs does not constitute a stable reproductive barrier

  • Ondřej Balvín
  • Tomáš Bartonička
  • Kateřina Pilařová
  • Zachary DeVries
  • Coby Schal
Original Paper

Abstract

The common bed bug Cimex lectularius, has been recently shown to constitute two host races, which are likely in the course of incipient speciation. The human-associated lineage splits from the ancestral bat-associated species deep in the history of modern humans, likely even prior to the Neolithic Period and establishment of the first permanent human settlements. Hybridization experiments between these two lineages show that post-mating reproductive barriers are incomplete due to local variation. As mating takes place in off-host refugia marked by aggregation semiochemicals, the present investigation tested the hypothesis that bed bugs use these semiochemicals to differentiate between refugia marked by bat- and human-associated bed bugs; this would constitute a pre-copulation isolation mechanism. The preference for lineage-specific odors was tested using artificial shelters conditioned by a group of either male or female bed bugs. Adult males were assayed individually in four-choice assays that included two clean unconditioned control shelters. In most assays, bed bugs preferred to rest in conditioned shelters, with no apparent fidelity to shelters conditioned by their specific lineage. However, 51 % of the bat-associated males preferred unconditioned shelters over female-conditioned shelters of either lineage. Thus, bed bugs show no preferences for lineage-specific shelters, strongly suggesting that semiochemicals associated with shelters alone do not function in reproductive isolation.

Keywords

Pre-copulation reproduction isolation Pheromones Parasites Aggregation behavior 

References

  1. Aak A, Rukke BA (2014) Bed bugs, their blood sources and life history parameters: a comparison of artificial and natural feeding: artificial feeding of bed bugs. Med Vet Entomol 28:50–59. doi:10.1111/mve.12015 CrossRefPubMedGoogle Scholar
  2. Adelman ZN, Kilcullen KA, Koganemaru R, Anderson MAE, Anderson TD, Miller DM (2011) Deep sequencing of pyrethroid-resistant bed bugs reveals multiple mechanisms of resistance within a single population. PLoS ONE 6:e26228. doi:10.1371/journal.pone.0026228 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Balvín O, Munclinger P, Kratochvíl L, Vilímova J (2012) Mitochondrial DNA and morphology show independent evolutionary histories of bedbug Cimex lectularius (Heteroptera: Cimicidae) on bats and humans. Parasitol Res 111:457–469CrossRefPubMedGoogle Scholar
  4. Booth W, Balvín O, Vargo EL, Vilímová J, Schal C (2015) Host association drives genetic divergence in the bed bug, Cimex lectularius. Mol Ecol 24:980–992. doi:10.1111/mec.13086 CrossRefPubMedGoogle Scholar
  5. Bournez L, Cangi N, Lancelot R, Pleydell DRJ, Stachurski F, Bouyer J, Martinez D, Lefrançois T, Neves L, Pradel J (2015) Parapatric distribution and sexual competition between two tick species, Amblyomma variegatum and A. hebraeum (Acari, Ixodidae), in Mozambique. Parasit Vectors. doi: 10.1186/s13071-015-1116-7
  6. Choe DH, Campbell K (2014) Effect of feeding status on mortality response of adult bed bugs (Hemiptera: Cimicidae) to some insecticide products. J Econ Entomol 107:1206–1215. doi:10.1603/EC13478 CrossRefPubMedGoogle Scholar
  7. Condò SG, El-Sherbini S, Shehata YM, Corda M, Pellegrini MG, Brix O, Giardina B (1989) Hemoglobins from bats (Myotis myotis and Rousettus aegyptiacus): a possible example of molecular adaptation to different physiological requirements. Biol Chem Hoppe Seyler 370:861–867CrossRefPubMedGoogle Scholar
  8. Dumas P, Legeai F, Lemaitre C, Scaon E, Orsucci M, Labadie K, Gimenez S, Clamens AL, Henri H, Vavre F, Aury JM, Fournier P, Kergoat GJ, d’Alençon E (2015) Spodoptera frugiperda (Lepidoptera: Noctuidae) host-plant variants: two host strains or two distinct species? Genetica 143:305–316. doi:10.1007/s10709-015-9829-2 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Etges WJ, de Oliveira CC (2014) Premating isolation is determined by larval rearing substrates in cactophilic Drosophila mojavensis. X. Age-specific dynamics of adult epicuticular hydrocarbon expression in response to different host plants. Ecol Evol n/a-n/a. doi: 10.1002/ece3.1088
  10. Gries R, Britton R, Holmes M, Zhai H, Draper J, Gries G (2015) Bed bug aggregation pheromone finally identified. Angew Chem Int Ed 54:1135–1138. doi:10.1002/anie.201409890 CrossRefGoogle Scholar
  11. Horáček I (1983) Remarks on the causality of population decline in European bats. Myotis 21–22:138–147Google Scholar
  12. Horváth G (1913) La distribution géographique des cimicides et l´origine des punaises des lits. Extr IXe Congr Int Zool Tenu Monaco 294–299.Google Scholar
  13. Jennings JH, Etges WJ, Schmitt T, Hoikkala A (2014) Cuticular hydrocarbons of Drosophila montana: geographic variation, sexual dimorphism and potential roles as pheromones. J Insect Physiol 61:16–24. doi:10.1016/j.jinsphys.2013.12.004 CrossRefPubMedGoogle Scholar
  14. Lecocq T, Coppée A, Mathy T, Lomme P, Cammaerts-Tricot MC, Urbanová K, Valterová I, Rasmont P (2015) Subspecific differentiation in male reproductive traits and virgin queen preferences, in Bombus terrestris. Apidologie 46:595–605. doi:10.1007/s13592-015-0349-y CrossRefGoogle Scholar
  15. Levinson H, Bar AI (1971) Assembling and alerting scents produced by the bedbug, Cimex lectularius L. Experientia 27:102–103CrossRefPubMedGoogle Scholar
  16. Mamidala P, Rajarapu SP, Jones SC, Mittapalli O (2011) Identification and validation of reference genes for quantitative real-time polymerase chain reaction in Cimex lectularius. J Med Entomol 48:947–951CrossRefPubMedGoogle Scholar
  17. Olivero PA, Gonzalez A, Mattoni CI, Peretti AV (2015) Chemical caresses: geographical variation of male sexual signals in a Neotropical scorpion. Behaviour 152:12–13CrossRefGoogle Scholar
  18. Olson JF, Moon RD, Kells SA (2008) Off-host aggregation behavior and sensory basis of arrestment by Cimex lectularius (Heteroptera: Cimicidae). J Insect Physiol 55:580–587CrossRefGoogle Scholar
  19. Olson JF, Moon RD, Kells SA, Mesce KA (2014) Morphology, ultrastructure and functional role of antennal sensilla in off-host aggregation by the bed bug, Cimex lectularius. Arthropod Struct Dev 43:117–122. doi:10.1016/j.asd.2013.12.004 CrossRefPubMedGoogle Scholar
  20. Povolný D, Usinger RL (1966) The discovery of a possibly aboriginal population of the bed bug (Cimex lectularius Linnaeus, 1958). Acta Musei Morav Sci Nat 51:237–242Google Scholar
  21. Robison GA, Balvin O, Schal C, Vargo EL, Booth W (2015) Extensive mitochondrial heteroplasmy in natural populations of a resurging human pest, the bed bug (Hemiptera: Cimicidae). J Med Entomol 52:734–738. doi:10.1093/jme/tjv055 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Servedio MR, Noor MAF (2003) The role of reinforcement in speciation: theory and data. Annu Rev Ecol Evol Syst 34:339–364CrossRefGoogle Scholar
  23. Siljander E, Penman D, Harlan H, Gries G (2007) Evidence for male- and juvenile-specific contact pheromones of the common bed bug Cimex lectularius. Entomol Exp Appl 125:215–219CrossRefGoogle Scholar
  24. Siljander E, Gries R, Khaskin G, Gries G (2008) Identification of the airborne aggregation pheromone of the common bed bug, Cimex lectularius. J Chem Ecol 37:708–718CrossRefGoogle Scholar
  25. Smadja C, Butlin RK (2009) On the scent of speciation: the chemosensory system and its role in premating isolation. Heredity 102:77–97CrossRefPubMedGoogle Scholar
  26. StatSoft I (2007) STATISTICA (data analysis software system), version 8.0. www.statsoft.com.
  27. Thomas Y, Bethenod MT, Pelozuelo L, Frerot B, Bourguet D (2005) Genetic isolation between two sympatric host-plant races of the European corn borer, Ostrinia nubilalis Hubner. I. Sex pheromone, moth emergence timing, and parasitism. Evolution 57:261–273Google Scholar
  28. Usinger RL (1966) Monograph of Cimicidae. Entomological Society of America, Washington, D.C., United States.Google Scholar
  29. Wada-Katsumata A, Zurek L, Nalyanya G, Roelofs WL, Zhang A, Schal C (2015) Gut bacteria mediate aggregation in the German cockroach. Proc Natl Acad Sci 201504031. doi: 10.1073/pnas.1504031112
  30. Wawrocka K, Bartonička T (2013) Two different lineages of bedbug (Cimex lectularius) reflected in host specificity. Parasitol Res 112:3897–3904CrossRefPubMedGoogle Scholar
  31. Wawrocka K, Balvín O, Bartonička T (2015) Reproduction barrier between two lineages of bed bug (Cimex lectularius) (Heteroptera: Cimicidae). Parasitol Res 114:3019–3025. doi:10.1007/s00436-015-4504-1 CrossRefPubMedGoogle Scholar
  32. Werren JH (1997) Biology of Wolbachia. Annu Rev Entomol 42:587–609CrossRefPubMedGoogle Scholar
  33. Zhu F, Wigginton J, Romero A, Moore A, Ferguson K, Palli R, Potter MF, Haynes KF, Palli SR (2010) Widespread distribution of knockdown resistance mutations in the bed bug, Cimex lectularius (Hemiptera: Cimicidae), populations in the United States. Arch Insect Biochem Physiol 73:245–257PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Ondřej Balvín
    • 1
  • Tomáš Bartonička
    • 2
  • Kateřina Pilařová
    • 1
  • Zachary DeVries
    • 3
  • Coby Schal
    • 3
  1. 1.Department of Ecology, Faculty of Environmental SciencesCzech University of Life Sciences PraguePrague 6Czech Republic
  2. 2.Department of Botany and ZoologyMasaryk UniversityBrnoCzech Republic
  3. 3.Department of Entomology and Plant PathologyNorth Carolina State UniversityRaleighUSA

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