Parasitology Research

, Volume 111, Issue 1, pp 457–469 | Cite as

Mitochondrial DNA and morphology show independent evolutionary histories of bedbug Cimex lectularius (Heteroptera: Cimicidae) on bats and humans

  • Ondřej BalvínEmail author
  • Pavel Munclinger
  • Lukáš Kratochvíl
  • Jitka Vilímová
Original Paper


The bedbug, Cimex lectularius, is a well-known human ectoparasite that is reemerging after a long absence of several decades in developed countries of North America and Western Europe. Bedbugs’ original hosts were likely bats, and the bedbugs are still common in their roosts. Using morphometry and sequences of mitochondrial cytochrome oxidase subunit I and 16S genes, we showed that the populations on bats and humans are largely isolated and differ in morphology. The character of the morphological difference suggests it to be due to adaptation to different hosts, namely adaptations to different sensory, feeding, and dispersal needs. Using the molecular data, we estimated the time of splitting into bat- and human-parasitizing groups using the isolation-with-migration model. The estimate is surprisingly long ago and seems to predate the expansion of modern human from Africa. The gene flow between bat- and human-parasitizing bedbugs is limited and asymmetric with prevailing direction from human-parasitizing populations to bat-parasitizing populations. The differentiation of the populations fits the concept of host races and supports the idea of sympatric speciation. Furthermore, our findings contradict recently formulated hypotheses suggesting bat roosts as a source of bedbug’s resurgence as a human pest. Also, we extend the known host range of the bedbug by two bat species.


Migration Rate Effective Population Size Discriminant Function Analysis Original Host Host Association 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Unfortunately, we cannot name all the far more than 100 people who have taken part in collecting bedbug material for the study. We express our deepest thanks to all of them! We are thankful for help with lab work and comments on the manuscript from Josef Bryja, Jan Zima (Academy of Sciences, Czech Republic), Petr Janšta, Jakub Straka (Charles University, Czech Republic), and Martina Komárková (Institute of Animal Science, Prague, Czech Republic). We would like to express our gratitude to Gale Allen Kirking (English Editorial Services, Brno) for the correction of English. The study was supported by the Ministry of Education, Youth and Sports of the Czech Republic (project no. MSM 0021620828) and a grant from the Grant Agency of Charles University (no. 2010/45610).

Supplementary material

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ESM 1 (XLS 36 kb)
436_2012_2862_MOESM2_ESM.doc (22 kb)
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  1. Abul-Hab J (1979) On the bed bugs (Hemiptera, Cimicidae) in Iraq. Iraq Bull End Dis 19(1–4):65–76Google Scholar
  2. Als TD, Nash DR, Boomsma JJ (2002) Geographical variation in host-ant specificity of the parasitic butterfly Maculinea alcon in Denmark. Ecol Entomol 27(4):403–414CrossRefGoogle Scholar
  3. Armitage SJ, Jasim SA, Marks AE, Parker AG, Usik VI, Uerpmann HP (2011) The southern route “out of Africa”: evidence for an early expansion of modern humans into Arabia. Science 331:453–456PubMedCrossRefGoogle Scholar
  4. Aulagnier S, Haffner P, Mitchell-Jones AJ, Moutou F, Zima J (2008) Mammals of Europe, North Africa and the Middle East. Delachaux & Niestlé, ParisGoogle Scholar
  5. Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16(1):37–48PubMedCrossRefGoogle Scholar
  6. Bartonička T (2008) Cimex pipistrelli (Heteroptera, Cimicidae) and the dispersal propensity of bats: an experimental study. Parasitol Res 104:163–168PubMedCrossRefGoogle Scholar
  7. Bartonička T, Gaisler J (2007) Seasonal dynamics in the number of parasitic bugs (Heteroptera, Cimicidae): a possible cause of roost switching in bats (Chiroptera: Vespertilionidae). Parasitol Res 100:1323–1330PubMedCrossRefGoogle Scholar
  8. Berrilli F, D’Amelio S, Rossi L (2002) Ribosomal and mitochondrial DNA sequence variation in Sarcoptes mites from different hosts and geographical regions. Parasitol Res 88(8):772–777PubMedCrossRefGoogle Scholar
  9. Bobkova O (2001) Ectoparasitic fauna of migrant and residental bat species. Novitates Theriologicae 6:81–84Google Scholar
  10. Bogdanowitz W (1994) Myotis daubentonii. Mammal Species 475:1–9CrossRefGoogle Scholar
  11. Brower AVZ (1994) Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. PNAS 91:6491–6495PubMedCrossRefGoogle Scholar
  12. Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, SunderlandGoogle Scholar
  13. Derricourt R (2006) Getting “out of Africa”: sea crossings, land crossings and culture in the hominin migrations. J World Prehist 19:119–132CrossRefGoogle Scholar
  14. Dick CW, Esberard CEL, Graciolli G, Bergallo HG, Gettinger D (2009) Assessing host specificity of obligate ectoparasites in the absence of dispersal barriers. Parasitol Res 105(5):1345–1349PubMedCrossRefGoogle Scholar
  15. Doggett SL, Geary MJ, Russell RC (2004) The resurgence of bed bugs in Australia: with notes on their ecology and control. Environ Health 4(2):30–38Google Scholar
  16. Dres M, Mallet J (2002) Host races in plant-feeding insects and their importance in sympatric speciation. Phil Trans R Soc B 357(1420):471–492PubMedCrossRefGoogle Scholar
  17. Dubinij VB (1947) Ekologičeskije nabljudjenija nad krovososuščimi klopami sem. Cimicidae Daurskoj stepi. [Ecological remarks to bloodsucking bugs of the family Cimicidae of Daur steppe] (in Russian). Entomologičeskoje obozrenije 39(3–4):232–246Google Scholar
  18. Eichler W (1937) Über die bei europäischer Vögeln vorkommenden Wanzenarten. Zool Anz 120(11–12):267–271Google Scholar
  19. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50Google Scholar
  20. Farris JS, Kallersjo M, Kluge AG, Bult C (1995) Testing significance of incongruence. Cladistics 10:315–319CrossRefGoogle Scholar
  21. Feroz M (1969) Toxicological and genetical studies of organophosphorus-resistance in Cimex lectularius L. Bull Entomol Res 59(1968):377–382PubMedCrossRefGoogle Scholar
  22. Full RJ, Tu MS (1990) Mechanics of a rapid running insect: two-, four- and six-legged locomotion. J Exp Biol 156:215–231Google Scholar
  23. Hafner MS, Sudman PD, Villablanca FX, Spradling TA, Demastes JD, Nadler SA (1994) Disparate rates of molecular evolution in cospeciating hosts and parasites. Science 265:1087–1090PubMedCrossRefGoogle Scholar
  24. Hajibabaei M, Janzen DH, Burns JM, Hallwachs W, Hebert PDN (2006) DNA barcodes distinguish species of tropical Lepidoptera. PNAS 103(4):968–971PubMedCrossRefGoogle Scholar
  25. Hey J, Nielsen R (2004) Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747–760PubMedCrossRefGoogle Scholar
  26. Hey J, Nielsen R (2007) Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. PNAS 104:2785–2790PubMedCrossRefGoogle Scholar
  27. Horáček I (1983–4) Remarks on the causality of population decline in European bats. Myotis 21–22:138–147Google Scholar
  28. Horváth G (1913) La distribution géographique des cimicides et l´origine des punaises des lits. Extrait du IXe Congres International de Zoologie Tenu a Monaco, pp 294–299Google Scholar
  29. Huson DH, Rupp R, Scornavacca C (2010) Phylogenetic networks. Cambridge, CambridgeCrossRefGoogle Scholar
  30. Hwang SW, Svoboda TJ, De Yong IJ, Kabasele KJ, Gogosis E (2005) Bed bug infestation in an urban environment. Emerg Infect Dis 11(4):533–538PubMedCrossRefGoogle Scholar
  31. Jackson DA (1993) Stopping rules in principal component analysis: a comparison of statistical and heuristic approaches. Ecology 74(8):2204–2214CrossRefGoogle Scholar
  32. Johnson CG (1939) Taxonomic characters, variability, and relative growth in Cimex lectularius L. and C. columbarius Jenyns (Heteropt. Cimicidae). Trans R Entomol Soc Lond 89(2):543–568Google Scholar
  33. Johnson CG (1941) The ecology of the bed-bug, Cimex lectularius L., in Britain. J Hyg 41(4):345–361CrossRefGoogle Scholar
  34. Johnson KP, Cruickshank RH, Adams RJ, Smith VS, Page RDM, Clayton DH (2003) Dramatically elevated rate of mitochondrial substitution in lice (Insecta: Phthiraptera). Mol Phyl Evol 26:231–242CrossRefGoogle Scholar
  35. Kambhampati S, Smith PT (1995) PCR primers for the amplification of four insect mitochondrial gene fragments. Insect Mol Biol 4:223–236CrossRefGoogle Scholar
  36. Katoh K, Asimenos G, Toh H (2009) Multiple alignment of DNA sequences with MAFFT methods. Mol Biol 537:39–64Google Scholar
  37. Kilpinen O, Kristensen M, Jensen KMV (2011) Resistance differences between chlorpyrifos and synthetic pyrethroids in Cimex lectularius population from Denmark. Parasitol Res 109(5):1461–1464PubMedCrossRefGoogle Scholar
  38. Krasnov BR, Korine C, Burdelova NV, Khokhlova IS, Pinshow B (2007) Between-host phylogenetic distance and feeding efficiency in hematophagous ectoparasites: rodent fleas and a bat host. Parasitol Res 101(2):365–371PubMedCrossRefGoogle Scholar
  39. Kuhner MK (2008) Coalescent genealogy samplers: windows into population history. Trends Ecol Evol 24:86–93PubMedCrossRefGoogle Scholar
  40. Langmore NE, Maurer G, Adcock GJ, Kilner RM (2008) Socially acquired host-specific mimicry and the evolution of host races in Horsfield’s bronze-cuckoo Chalcites basalis. Evolution 62(7):1689–1699PubMedCrossRefGoogle Scholar
  41. Lanza B (1999) I parassiti dei pipistrelli (Mammalia, Chiroptera) della fauna italiana. Monographie 30. Museo Regionale di Scienze Naturali, TurinGoogle Scholar
  42. Light JE, Reed DL (2008) Multigene analysis of phylogenetic relationships and divergence times of primate sucking lice (Phthiraptera: Anoplura). Mol Phyl Evol 50:376–390CrossRefGoogle Scholar
  43. Lýsek H (1966) Neobvyklé způsoby šíření Cimex lectularius. [Unusual ways of dispersal of Cimex lectularius] (in Czech). Československá. Hygiena 11(10):617–620Google Scholar
  44. Marchetti K, Nakamura H, Gibbs HL (1998) Host-race formation in the common cuckoo. Science 282(5388):471–472PubMedCrossRefGoogle Scholar
  45. McCoy KD, Tirard C, Michalakis Y (2003) Spatial genetic structure of the ectoparasite Ixodes uriae within breeding cliffs of its colonial seabird host. Heredity 91:422–429PubMedCrossRefGoogle Scholar
  46. Nielsen R, Beaumont MA (2009) Statistical inferences in phylogeography. Mol Eco 18:1034–1047CrossRefGoogle Scholar
  47. Nielsen R, Wakeley J (2001) Distinguishing migration from isolation. A Markov chain Monte Carlo approach. Genetics 158:885–896PubMedGoogle Scholar
  48. Poppius B (1912) Cimex verspertilionis n.sp. Acta Soc Fauna Flora Fenn 38:56–58Google Scholar
  49. Povolný D (1957) Kritická studie o štěnicovitých (Het. Cimicidae) v Československu. [Review study on cimicids (Het. Cimicidae) in Czechoslovakia] (in Czech). Folia Zool 6 (10) (1):59–80Google Scholar
  50. Povolný D (1959) Rozšíření a původ štěnice obecné. [Distribution and origin of the bed bug] (in Czech). Živa 1959 (45):225–226Google Scholar
  51. Povolný D, Usinger RL (1966) The discovery of a possibly aboriginal population of the bed bug (Cimex lectularius Linnaeus, 1958). Acta Mus Moraviae, Sci biol 51:237–242Google Scholar
  52. Protić L, Paunović M (2006) Bat bugs Cimex dissimilis (Horváth, 1910) (Heteroptera: Cimicidae)—the first record from Serbia. In: Abstracts, 3rd meeting of International Heteropterological Society, Wageningen, NetherlandsGoogle Scholar
  53. Reed DL, Smith VS, Hammond SL, Rogers AL, Clayton DH (2004) Genetic analysis of lice supports direct contact between modern and archaic humans. PLOS Biology 2(11):1973–1983CrossRefGoogle Scholar
  54. Reinhardt K, Siva-Jothy MT (2007) Biology of the bed bugs (Cimicidae). Annu Rev Entomol 52:351–374PubMedCrossRefGoogle Scholar
  55. Reinhardt K, Harder A, Holland S, Hooper J, Leake-Lyall C (2008) Who knows the bed bug? Knowledge of adult bed bug appearance increases with people age in three counties of Great Britain. J Med Entomol 45(5):956–958PubMedCrossRefGoogle Scholar
  56. Romero A, Potter MF, Haynes KF (2007) Insecticide resistance in the bedbugs: a factor in the pest sudden resurgence? J Med Entomol 44(2):175–178PubMedCrossRefGoogle Scholar
  57. Rybin N, Horáček I, Červený J (1989) Bats of southern Kirghizia: distribution and faunal status. In: Hanák V, Horáček I, Gaisler J (eds) European bat research 1987. Charles University Press, Prague, pp 421–441Google Scholar
  58. Sailer R (1952) The bedbug. An old bedfellow that´s still with us. Pest control 10 (20):22, 24, 70, 72Google Scholar
  59. Shea JJ (2008) Transitions or turnovers? Climatically-forced extinctions of Homo sapiens and Neanderthals in the east Mediterranean Levant. Quaternary Sci Rev 27:2253–2270CrossRefGoogle Scholar
  60. Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87(6):651–701Google Scholar
  61. Simov N, Ivanova T, Schunger I (2006) Bat-parasitic Cimex species (Hemiptera: Cimicidae) on the Balkan Peninsula, with zoogeographical remarks on Cimex lectularius, Linnaeus. Zootaxa 2006(1190):59–68Google Scholar
  62. Slack HD (1937) Notes on Scottish Hemiptera–Heteroptera. Scottish Naturalist 225(91)Google Scholar
  63. StatSoft I (2007) STATISTICA (data analysis software system), version 8.0. Accessed 01 Dec 2009
  64. Swofford DL (1999) PAUP* Phylogenetic analysis using parsimony; version 4. Sinauer Associates, SunderlandGoogle Scholar
  65. Szalanski AL, Austin JW, McKern JA, Steelman CD, Gold RE (2008) Mitochondrial and ribosomal internal transcribed spacer 1 diversity of Cimex lectularius (Hemiptera: Cimicidae). J Med Entomol 45(2):229–236PubMedCrossRefGoogle Scholar
  66. Ting L, Blickhan R, Full RJ (1994) Dynamic and static stability in hexapedal runners. J Exp Biol 197:251–269PubMedGoogle Scholar
  67. Ueshima N (1964) Experiments on reproductive isolation in Cimex lectularius and Cimex columbarius (Hemiptera: Cimicidae). Pan-Pac Entomol 40(1):47–53Google Scholar
  68. Usinger RL (1966) Monograph of Cimicidae. Entomological Society of America, Washington, D.CGoogle Scholar
  69. Wagner E (1967) Wanzen oder Heteropteren II. Cimicomorpha, vol 55. Die Tierwelt Deutschlands und der angrenzenden Meeresteile. Gustav Fischer, JenaGoogle Scholar
  70. Walter G (2004) Űberblick zum Vorkommen und zur Biologie von Ectoparasiten (Siphonaptera; Cimicidae; Nycteribiidae; Calliphoridae) bei Fledermäusen in Deutschland. Nyctalus 9(5):460–476Google Scholar
  71. Weidner H (1958) Die Entstehung der Hausinsekten. Z Angew Entomol 42:429–447CrossRefGoogle Scholar
  72. 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 73(4):245–257Google Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Ondřej Balvín
    • 1
    Email author
  • Pavel Munclinger
    • 1
  • Lukáš Kratochvíl
    • 2
  • Jitka Vilímová
    • 1
  1. 1.Department of Zoology, Faculty of ScienceCharles UniversityPrague 2Czech Republic
  2. 2.Department of Ecology, Faculty of ScienceCharles UniversityPrague 2Czech Republic

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