Parasitology Research

, Volume 111, Issue 1, pp 393–401 | Cite as

Evolutionary co-variation of host and parasite diversity—the first test of Eichler’s rule using parasitic lice (Insecta: Phthiraptera)

  • Zoltán VasEmail author
  • Gábor Csorba
  • Lajos Rózsa
Original Paper


The taxonomic richness of lice (Phthiraptera) varies considerably among their avian and mammalian hosts. Previous studies explored some factors shaping louse diversity; however, the so-called Eichler’s rule—according to which taxonomic richness of parasites co-varies with that of their hosts—has never been tested. Our study incorporates all families of birds and mammals and the whole order of lice to test this co-variation, thus we present the widest taxonomic range to test any correlates of louse richness. Louse richness data were controlled for uneven sampling effort. We used the method of independent contrasts to control for phylogenetic effects. We found a strong correlation between the species richness of avian and mammalian families and generic richness of their lice. We discuss some alternative macroevolutionary and macroecological hypotheses that may explain this phenomenon that may well be a general feature of parasitism and it seems possible that this effect contribute considerably to global biodiversity.


Taxonomic Richness Generic Richness Taxonomical Distinctness Parasite Diversity Host Family 
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.



We are grateful to Dr. Olaf R. P. Bininda-Emonds for kindly sending us a nexus format of their family-level mammalian tree. We thank Anikó Kovács-Hostyánszki for translating German papers. We would like to express our gratitude to Dr. Thomas Cooper (Eszterházy Károly College, Dept. of American Studies) for the linguistic corrections.


  1. Agapow P-M, Isaac NJB (2002) MacoCAIC, revealing correlates of species richness by comparative analysis. Divers Distrib 8:41–43CrossRefGoogle Scholar
  2. Barbosa A, Merino S, de Lope F, Møller AP (2002) Effects of feather lice on flight behavior of male barn swallows (Hirundo rustica). Auk 119:213–216CrossRefGoogle Scholar
  3. Barker FK, Cibois A, Schikler P, Feinstein J, Cracraft J (2004) Phylogeny and diversification of the largest avian radiation. Proc Natl Acad Sci U S A 101:11040–11045PubMedCrossRefGoogle Scholar
  4. Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A (2007) The delayed rise of present-day mammals. Nature 446:507–512PubMedCrossRefGoogle Scholar
  5. Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A (2008) Corrigendum, the delayed rise of present-day mammals. Nature 456:274CrossRefGoogle Scholar
  6. Booth DT, Clayton DH, Block BA (1993) Experimental demonstration of the energetic cost of parasitism in free-ranging hosts. Proc R Soc Lond B 253:125–129CrossRefGoogle Scholar
  7. Bordes F, Morand S (2009) Parasite diversity, an overlooked measure of parasitic pressures? Oikos 118:801–806CrossRefGoogle Scholar
  8. Bordes F, Morand S, Krasnov BR (2011) Does investment into “expensive” tissue compromise anti-parasitic defence? Testes size, brain size and parasite diversity in rodent hosts. Oecologia 165(1):7–16PubMedCrossRefGoogle Scholar
  9. Brown CR, Brown MB, Rannala B (1995) Ectoparasites reduce long-term survivorship of their avian host. Proc R Soc Lond B 262:313–319CrossRefGoogle Scholar
  10. Clay T (1964) Geographical distribution of the Mallophaga (Insecta). Bull Br Ornithol Club 84:14–16Google Scholar
  11. Clayton DH (1990) Mate choice in experimentally parasitized rock doves, lousy males lose. Am Zool 30:251–262Google Scholar
  12. Clayton DH, Walther BA (2001) Infuence of host ecology and morphology on the diversity of neotropical bird lice. Oikos 95:455–467CrossRefGoogle Scholar
  13. Clayton DH, Adams RJ, Bush SE (2008) Phthiraptera, the chewing Lice. In: Atkinson CT, Thomas NJ, Hunter DB (eds) Parasitic diseases of wild birds. Wiley-Blackwell, Ames, pp 515–526Google Scholar
  14. Clayton DH, Koop JAH, Harbison CW, Moyer BR, Bush SE (2010) How birds combat ectoparasites. Open Ornithol J 3:41–71Google Scholar
  15. R Development Core Team (2010) R, A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available at
  16. Diaz-Uriarte R, Garland T Jr (1996) Testing hypotheses of correlated evolution using phylogenetically independent contrasts, sensitivity to deviations from Brownian motion. Syst Biol 45:27–47CrossRefGoogle Scholar
  17. Diaz-Uriarte R, Garland T Jr (1998) Effects of branch length errors on the performance of phylogenetically independent contrasts. Syst Biol 47:654–672PubMedCrossRefGoogle Scholar
  18. Dickinson E (ed) (2003) The Howard and Moore complete checklist of the birds of the world, 3rd edn. Christopher Helm, LondonGoogle Scholar
  19. Dunning JB (ed) (2008) CRC handbook of avian body masses, 2nd edn. CRC, Boca RatonGoogle Scholar
  20. Durden LA, Musser GG (1994) The mammalian hosts of the sucking lice (Anoplura) of the world, a host–parasite list. Bull Soc Vector Ecol 19(2):130–168Google Scholar
  21. Eichler W (1942) Die Entfaltungsregel und andere Gesetzmäßigkeiten in den parasitogenetischen Beziehungen der Mallophagen und anderer ständiger Parasiten zu ihren Wirten. Zool Anz 137:77–83Google Scholar
  22. Fahrenholz H (1913) Ectoparasiten und abstammungslehre. Zool Anz 41:371–374Google Scholar
  23. Faraway J (2009) faraway, Functions and datasets for books by Julian Faraway. R package version 1.0.4. Available at
  24. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15CrossRefGoogle Scholar
  25. Felsenstein J (2004) Inferring phylogenies. Sinauer Associates, SunderlandGoogle Scholar
  26. Felső B, Rózsa L (2006) Reduced taxonomic richness of lice (Insecta, Phthiraptera) in diving birds. J Parasitol 92:867–869PubMedCrossRefGoogle Scholar
  27. Felső B, Rózsa L (2007) Diving behavior reduces generic richness of lice (Insecta, Phthiraptera) of mammals. Acta Parasitol 52(1):82–85CrossRefGoogle Scholar
  28. Freckleton RP (2002) On the misuse of residuals in ecology, regression of residuals vs. multiple regressions. J Anim Ecol 71:542–545CrossRefGoogle Scholar
  29. Freckleton RP (2009) The seven deadly sins of comparative analysis. J Evol Biol 22:1367–1375PubMedCrossRefGoogle Scholar
  30. Garland T Jr, Díaz-Uriarte R (1999) Polytomies and phylogenetically independent contrasts, examination of the bounded degrees of freedom approach. Syst Biol 48:547–558PubMedCrossRefGoogle Scholar
  31. Garland T Jr, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32Google Scholar
  32. Gregory RD (1990) Parasites and host geographic range as illustrated by waterfowl. Func Ecol 4(5):645–654CrossRefGoogle Scholar
  33. Hackett SJ, Kimball RT, Reddy S, Bowie RCK, Braun EL, Braun J, Chojnowski JL, Cox WA, Han KL, Harshman J, Huddleston CJ, Marks BD, Miglia KJ, Moore WS, Sheldon FH, Steadman DW, Witt CC, Yuri T (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320:1763–1768PubMedCrossRefGoogle Scholar
  34. Hellenthal RA, Price RD (1991) Biosystematics of the chewing lice of pocket gophers. Ann Rev Entomol 36:185–203CrossRefGoogle Scholar
  35. Hughes J, Page RDM (2007) Comparative tests of ectoparasite species richness in seabirds. BMC Evol Biol 7:227PubMedCrossRefGoogle Scholar
  36. Johnson KP, Clayton DH (2003) The biology, ecology, and evolution of chewing lice. In: Price RD, Hellenthal RA, Palma RL, Johnson KP, Clayton DH (eds) The chewing lice, world checklist and biological overview. Illinois Natural History Survey Special Publication 24, Champaign, pp 449–476Google Scholar
  37. Johnson KP, Yoshizawa K, Smith VS (2004) Multiple origins of parasitism in lice. Proc R Soc Lond B 271:1771–1776CrossRefGoogle Scholar
  38. Kose M, Møller AP (1999) Sexual selection, feather breakage and parasites, the importance of white spots in the tail of the barn swallow. Behav Ecol Sociobiol 45:430–436CrossRefGoogle Scholar
  39. Kose M, Mand R, Møller AP (1999) Sexual selection for white tail spots in the barn swallow in relation to habitat choice by feather lice. Anim Behav 58:1201–1205PubMedCrossRefGoogle Scholar
  40. Krasnov BR (2008) Functional and evolutionary ecology of fleas, a model for ecological parasitology. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  41. Krasnov BR, Shenbrot GI, Khokhlova IS, Degen AA (2004) Flea species richness and parameters of host body, host geography and host “milieu”. J Anim Ecol 73:1121–1128CrossRefGoogle Scholar
  42. Krasnov BR, Shenbrot GI, Mouillot D, Khokhlova IS, Poulin R (2005) What are the factors determining the probability of discovering a flea species (Siphonaptera)? Parasitol Res 97:228–237PubMedCrossRefGoogle Scholar
  43. Krasnov BR, Korallo-Vinarskaya NP, Vinarski MV, Shenbrot GI, Mouillot D, Poulin R (2008) Searching for general patterns in parasite ecology, host identity vs. environmental influence on gamasid mite assemblages in small mammals. Parasitology 135:229–242PubMedGoogle Scholar
  44. Kuris AM, Blaustein AR, Alio JJ (1980) Hosts as islands. Am Nat 116:570–586CrossRefGoogle Scholar
  45. Macdonald D (ed) (2001) The new encyclopedia of mammals. Oxford University Press, OxfordGoogle Scholar
  46. MacLeod CJ, Paterson AM, Tompkins DM, Duncan RP (2010) Parasites lost—do invaders miss the boat or drown on arrival? Ecol Lett 13:516–527PubMedCrossRefGoogle Scholar
  47. Maddison WP, Maddison DR (2010) Mesquite, a modular system for evolutionary analysis version 2.74. Available at
  48. Mey E (2003) On the development of animal louse systematics (Insecta, Phthiraptera) up to the present day. Rudolstädter Naturhistorische Schriften 11:115–134Google Scholar
  49. Midford PE, Garland T Jr, Maddison WP (2010) PDAP,PDTREE package for Mesquite version 1.15. Available at
  50. Møller AP, Rózsa L (2005) Parasite biodiversity and host defenses, chewing lice and immune response of their avian hosts. Oecologia 142:169–176PubMedCrossRefGoogle Scholar
  51. Møller AP, Erritzøe J, Rózsa L (2010) A comparative analysis of the function of the uropygial gland in birds. Oecologia 163:303–311PubMedCrossRefGoogle Scholar
  52. Murrell A, Barker SC (2005) Multiple origins of parasitism in lice: phylogenetic analysis of SSU rDNA indicates that the Phthiraptera and Psocoptera are not monophyletic. Parasitol Res 97:274–280PubMedCrossRefGoogle Scholar
  53. Nelson BC (1972) A revision of the New World species of Ricinus (Mallophaga) occurring on Passeriformes (Aves). Univ Calif Publ Entomol 68:1–175Google Scholar
  54. Nowak RM (ed) (1999) Walker's mammals of the world, 6th edn. Johns Hopkins University Press, BaltimoreGoogle Scholar
  55. Nunn CL, Altizer S, Sechrest W, Jones KE, Barton RA, Gittleman JL (2004) Parasites and the evolutionary diversification of primate clades. Am Nat 164:90–103CrossRefGoogle Scholar
  56. Page RDM (ed) (2003) Tangled trees—phylogeny, cospeciation, and coevolution. University of Chicago Press, ChicagoGoogle Scholar
  57. Papp PL, Tökölyi J, Szép T (2005) Frequency and consequences of feather holes in Barn Swallows Hirundo rustica. Ibis 147:169–175CrossRefGoogle Scholar
  58. Paterson AM, Palma RL, Gray ER (1999) How frequently do avian lice missing the boat? Implications for coevolutionary studies. Syst Biol 48:214–223CrossRefGoogle Scholar
  59. Perrins C (ed) (2003) The new encyclopedia of birds. Andromeda Oxford Ltd., OxfordGoogle Scholar
  60. Poulin R (2007) Evolutionary ecology of parasites. Princeton University Press, PrincetonGoogle Scholar
  61. Poulin R, Morand S (2004) Parasite biodiversity. Smithsonian Institution Press, Washington, D.CGoogle Scholar
  62. Price RD (1975) The Menacanthus eurysternus Complex (Mallophaga, Menoponidae) of the Passeriformes and Piciformes (Aves). Ann Entomol Soc Am 68(4):617–622Google Scholar
  63. Price RD, Hellenthal RA, Palma RL (2003) World checklist of chewing lice with host associations and keys to families and genera. In: Price RD, Hellenthal RA, Palma RL, Johnson KP, Clayton DH (eds) The chewing lice, world checklist and biological overview. Illinois Natural History Survey Special Publication 24, Champaign, pp 1–448Google Scholar
  64. Purvis A (1995) A composite estimate of primate phylogeny. Phil Trans R Soc Lond B 348:405–421CrossRefGoogle Scholar
  65. Purvis A, Garland T Jr (1993) Polytomies in comparative analyses of continuous data. Syst Biol 42:569–575CrossRefGoogle Scholar
  66. Raoult D, Roux V (1999) The body louse as a vector of reemerging human diseases. Clin Infect Dis 29:888–911PubMedCrossRefGoogle Scholar
  67. Reiczigel J, Harnos A, Solymosi N (2007) Biostatisztika nem statisztikusoknak [Biostatistics for non-statisticians]. Pars Kft, NagykovácsiGoogle Scholar
  68. Rheinwald G (1968) Die Mallophagengattung Ricinus De Geer, 1778. Revision der ausseramerikanischen Arten. Mitt Hambg Zool Mus Inst 65:181–326Google Scholar
  69. Rózsa L (1993) Speciation patterns of ectoparasites and “straggling” lice. Int J Parasitol 23:859–864PubMedCrossRefGoogle Scholar
  70. Rózsa L (1997a) Patterns in the abundance of avian lice (Phthiraptera, Amblycera, Ischnocera). J Avian Biol 28:249–254CrossRefGoogle Scholar
  71. Rózsa L (1997b) Wing feather mite (Acari, Proctophyllodidae) abundance correlates with body mass of Passerine hosts, a comparative study. Can J Zool 75:1535–1539CrossRefGoogle Scholar
  72. Silva M, Downing JA (eds) (1995) CRC handbook of mammalian body masses. CRC, Boca RatonGoogle Scholar
  73. Simberloff D, Dayan T (1991) The guild concept and the structure of ecological communities. Ann Rev Ecol Sys 22:115–143CrossRefGoogle Scholar
  74. Smith VS, Ford T, Johnson KP, Johnson PCD, Yoshizawa K, Light JE (2011) Multiple lineages of lice pass through the K–Pg boundary. Biol Lett. doi: 10.1098/rsbl.2011.0105
  75. Stammer HJ (1957) Gedanken zu den parasitophyletischen Regeln und zur Evolution der Parasiten. Zool Anz 159:255–267Google Scholar
  76. Sychra O, Najer T, Kounek F, Capek M, Literak I (2010) Chewing lice (Phthiraptera) on manakins (Passeriformes: Pipridae) from Costa Rica, with description of a new species of the genus Tyranniphilopterus (Phthiraptera: Philopteridae). Parasitol Res 106:925–931PubMedCrossRefGoogle Scholar
  77. Thomas F, Renaud F, Guégan JF (eds) (2005) Parasites and ecosystems. Oxford University Press, OxfordGoogle Scholar
  78. Vas Z, Lefebvre L, Johnson KP, Reiczigel J, Rózsa L (2011) Clever birds are lousy: co-variation between avian innovation and the taxonomic richness of their amblyceran lice. Int J Parasitol 41:1295–1300PubMedCrossRefGoogle Scholar
  79. Walther BA, Cotgreave P, Price RD, Gregory RD, Clayton DH (1995) Sampling effort and parasite species richness. Parasitol Today 11:306–310PubMedCrossRefGoogle Scholar
  80. Warwick RM, Clarke KR (1995) New ‘biodiversity’ measures reveal a decrease in taxonomic distinctness with increasing stress. Mar Ecol Prog Ser 129:301–305CrossRefGoogle Scholar
  81. Whiteman NK, Matson KD, Bollmer JL, Parker PG (2006) Disease ecology in the Galápagos Hawk (Buteo galapagoensis), host genetic diversity, parasite load and natural antibodies. Proc R Soc Lond B 273:797–804CrossRefGoogle Scholar
  82. Wilson DE, Reeder DM (eds) (2005) Mammal species of the world. A taxonomic and geographic reference, 3rd edn. Johns Hopkins University Press, BaltimoreGoogle Scholar
  83. Zuo X-H, Guo X-G, Zhan Y-Z, Wu D, Yang Z-H, Dong W-G, Huang L-Q, Ren T-G, Jing Y-G, Wang Q-H, Sun X-M, Lin S-J (2011) Host selection and niche differentiation in sucking lice (Insecta: Anoplura) among small mammals in southwestern China. Parasitol Res 108:1243–1251PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  1. 1.Department of Biomathematics and Informatics, Faculty of Veterinary SciencesSzent István UniversityBudapestHungary
  2. 2.Hungarian Natural History MuseumBudapestHungary
  3. 3.MTA-ELTE-MTM Ecology Research GroupBudapestHungary

Personalised recommendations