Experimental and Applied Acarology

, Volume 68, Issue 1, pp 21–31 | Cite as

Why do males choose heterospecific females in the red spider mite?

  • Yukie Sato
  • Heike Staudacher
  • Maurice W. Sabelis


In some species, males readily show courtship behaviour towards heterospecific females and even prefer them to females of their own species. This behaviour is generally explained by indiscriminate mating to acquire more mates, but may partly be explained by male mate preference mechanisms that have developed to choose among conspecific females, as male preference for larger females causes mating with larger heterospecific females. Recently, we found that males of the red spider mite, Tetranychus evansi collected from Spain (invasive population), prefer to mate with females of the two-spotted spider mite, T. urticae rather than with conspecific females. In spider mites, mate preference for non-kin individuals has been observed. Here, we investigated if T. evansi males collected from the area of its origin (Brazil) also show preference for heterospecific females. Secondly, we investigated if mate preference of T. evansi males for heterospecific females is affected by their relatedness to conspecific females which are offered together with heterospecific females. We found that mate preference for heterospecific females exists in Brazilian T. evansi, suggesting that the preference for heterospecific females is not a lack of evolved premating isolation with an allopatric species. We found that T. evansi males showed lower propensity to mate with heterospecific females when alternative females were non-kin in the two iso-female lines collected from Brazil. However, the effect of relatedness on male mate preference was not significant. We discuss alternative hypotheses explaining why T. evansi males prefer to mate with T. urticae females.


Heterospecific mating Inbreeding avoidance Invasive species Male mate choice Reproductive interference 



We thank Drs Arne Janssen, Merijn Kant, Juan Manuel Alba and Dan Li from the University of Amsterdam for the lines of spider mites, Mr. Ludek Tikovsky from the University of Amsterdam for the tomato plants, and Dr Johannes A. J. Breeuwer and Mr. Bart Schimmel from the University of Amsterdam for suggestions and primers in the check of endosymbiont infections in this study. HS was funded as a PhD candidate by the University of Amsterdam. YS was funded as a postdoc via the budget of MWS for the Royal Academy of Sciences (KNAW) professorship. YS activity in the University of Amsterdam was partly supported by the subsidy for the Program for Promoting the Enhancement of Research Universities, Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan, Researcher Dispatch and Invitation (etc.) Program, the University of Tsukuba—2014, Program III—Medium to Short-Term Overseas Dispatch Program.


  1. Allendorf FW, Lundquist LL (2003) Introduction: population biology, evolution, and control of invasive species. Conserv Biol 17:24–30. doi: 10.1046/j.1523-1739.2003.02365.x CrossRefGoogle Scholar
  2. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  3. Antolin MF (1999) A genetic perspective on mating systems and sex ratios of parasitoid wasps. Res Popul Ecol 41:29–37. doi: 10.1007/PL00011979 CrossRefGoogle Scholar
  4. Bitume EV, Bonte D, Ronce O et al (2013) Density and genetic relatedness increase dispersal distance in a subsocial organism. Ecol Lett 16:430–437. doi: 10.1111/ele.12057 CrossRefPubMedGoogle Scholar
  5. Bonduriansky R (2001) The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biol Rev Camb Philos Soc 76:305–339CrossRefPubMedGoogle Scholar
  6. Boubou A, Migeon A, Roderick GK et al (2012) Test of colonisation scenarios reveals complex invasion history of the red tomato spider mite Tetranychus evansi. PLoS ONE 7:e35601. doi: 10.1371/journal.pone.0035601 PubMedCentralCrossRefPubMedGoogle Scholar
  7. Boudreaux HB (1963) Biological aspects of some phytophagous mites. Annu Rev Entomol 8:137–154. doi: 10.1146/annurev.en.08.010163.001033 CrossRefGoogle Scholar
  8. Brückner D (1978) Why are there inbreeding effects in haplo-diploid systems? Evolution 32:456–458. doi: 10.2307/2407613 CrossRefGoogle Scholar
  9. Candolin U (2003) The use of multiple cues in mate choice. Biol Rev Camb Philos Soc 78:575–595CrossRefPubMedGoogle Scholar
  10. Crozier RH (1985) Adaptive consequences of male haploidy. In: Helle W, Sabelis MW (eds) Spider mites: their biology, natural enemies, and control, vol 1a. Elsevier, Amsterdam, pp 201–222Google Scholar
  11. Dame EA, Petren K (2006) Behavioural mechanisms of invasion and displacement in Pacific island geckos (Hemidactylus). Anim Behav 71:1165–1173. doi: 10.1016/j.anbehav.2005.10.009 CrossRefGoogle Scholar
  12. Faul F, Erdfelder E, Lang A-G, Buchner A (2007) G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 39:175–191. doi: 10.3758/BF03193146 CrossRefPubMedGoogle Scholar
  13. Faul F, Erdfelder E, Buchner A, Lang A-G (2009) Statistical power analyses using G*Power 3.1: tests for correlation and regression analyses. Behav Res Methods 41:1149–1160. doi: 10.3758/BRM.41.4.1149 CrossRefPubMedGoogle Scholar
  14. Ferragut F, Garzón-Luque E, Pekas A (2013) The invasive spider mite Tetranychus evansi (Acari: Tetranychidae) alters community composition and host-plant use of native relatives. Exp Appl Acarol 60:321–341. doi: 10.1007/s10493-012-9645-7 CrossRefPubMedGoogle Scholar
  15. Ferrero M, Calvo FJ, Atuahiva T et al (2011) Biological control of Tetranychus evansi Baker & Pritchard and Tetranychus urticae Koch by Phytoseiulus longipes Evans in tomato greenhouses in Spain [Acari: Tetranychidae, Phytoseiidae]. Biol Control 58:30–35. doi: 10.1016/j.biocontrol.2011.03.012 CrossRefGoogle Scholar
  16. Gröning J, Hochkirch A (2008) Reproductive interference between animal species. Q Rev Biol 83:257–282CrossRefPubMedGoogle Scholar
  17. Helle W (1967) Fertilization in the two-spotted spider mite (Tetranychus urticae: Acari). Entomol Exp Appl 10:103–110. doi: 10.1111/j.1570-7458.1967.tb00049.x CrossRefGoogle Scholar
  18. Helle W, Sabelis MW (1985) Spider mites. Their biology, natural enemies and control, vol 1. Elsevier, AmsterdamGoogle Scholar
  19. Hochkirch A, Deppermann J, Gröning J (2006) Visual communication behaviour as a mechanism behind reproductive interference in three pygmy grasshoppers (genus Tetrix, Tetrigidae, Orthoptera). J Insect Behav 19:559–571. doi: 10.1007/s10905-006-9043-2 CrossRefGoogle Scholar
  20. Hochkirch A, Gröning J, Bücker A (2007) Sympatry with the devil: reproductive interference could hamper species coexistence. J Anim Ecol 76:633–642. doi: 10.1111/j.1365-2656.2007.01241.x CrossRefPubMedGoogle Scholar
  21. Kozak GM, Reisland M, Boughmann JW (2009) Sex differences in mate recognition and conspecific preference in species with mutual mate choice. Evolution 63:353–365. doi: 10.1111/j.1558-5646.2008.00564.x CrossRefPubMedGoogle Scholar
  22. Mendelson TC, Shaw KL (2012) The (mis)concept of species recognition. Trends Ecol Evol 27:421–427. doi: 10.1016/j.tree.2012.04.001 CrossRefPubMedGoogle Scholar
  23. Navajas M, Lagnel J, Gutierrez J, Boursot P (1998) Species-wide homogeneity of nuclear ribosomal ITS2 sequences in the spider mite Tetranychus urticae contrasts with extensive mitochondrial COI polymorphism. Heredity 80(Pt 6):742–752CrossRefPubMedGoogle Scholar
  24. Navajas M, de Moraes GJ, Auger P, Migeon A (2012) Review of the invasion of Tetranychus evansi: biology, colonization pathways, potential expansion and prospects for biological control. Exp Appl Acarol 59:43–65. doi: 10.1007/s10493-012-9590-5 CrossRefPubMedGoogle Scholar
  25. Noor MAF (1996) Absence of species discrimination in Drosophila pseudoobscura and D. persimilis males. Anim Behav 52:1205–1210. doi: 10.1006/anbe.1996.0268 CrossRefGoogle Scholar
  26. Oku K (2008) Is only the first mating effective for females in the Kanzawa spider mite, Tetranychus kanzawai (Acari: Tetranychidae)? Exp Appl Acarol 45:53–57. doi: 10.1007/s10493-008-9157-7 CrossRefPubMedGoogle Scholar
  27. Oku K (2009) Female mating strategy during precopulatory mate guarding in spider mites. Anim Behav 77:207–211. doi: 10.1016/j.anbehav.2008.09.030 CrossRefGoogle Scholar
  28. Pfennig KS (1998) The evolution of mate choice and the potential for conflict between species and mate–quality recognition. Proc R Soc Lond B Biol Sci 265:1743–1748. doi: 10.1098/rspb.1998.0497 CrossRefGoogle Scholar
  29. Potter DA, Wrensch DL (1978) Interrupted matings and the effectiveness of second inseminations in the twospotted spider mite. Ann Entomol Soc Am 71:882–885. doi: 10.1093/aesa/71.6.882 CrossRefGoogle Scholar
  30. R Development Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  31. Saito Y, Sahara K, Mori K (2000) Inbreeding depression by recessive deleterious genes affecting female fecundity of a haplo-diploid mite. J Evol Biol 13:668–678. doi: 10.1046/j.1420-9101.2000.00198.x CrossRefGoogle Scholar
  32. Sakai AK, Allendorf FW, Holt JS et al (2001) The population biology of invasive specie. Annu Rev Ecol Syst 32:305–332CrossRefGoogle Scholar
  33. Sato Y, Alba JM, Sabelis MW (2014) Testing for reproductive interference in the population dynamics of two congeneric species of herbivorous mites. Heredity 113:495–502. doi: 10.1038/hdy.2014.53 PubMedCentralCrossRefPubMedGoogle Scholar
  34. Satoh Y, Yano S, Takafuji A (2001) Mating strategy of spider mite, Tetranychus urticae (Acari: Tetranychidae) males: postcopulatory guarding to assure paternity. Appl Entomol Zool 36:41–45. doi: 10.1303/aez.2001.41 CrossRefGoogle Scholar
  35. Tien NSH, Massourakis G, Sabelis MW, Egas M (2011) Mate choice promotes inbreeding avoidance in the two-spotted spider mite. Exp Appl Acarol 54:119–124. doi: 10.1007/s10493-011-9431-y PubMedCentralCrossRefPubMedGoogle Scholar
  36. Tien NSH, Sabelis MW, Egas M (2015) Inbreeding depression and purging in a haplodiploid: gender-related effects. Heredity 114:327–332. doi: 10.1038/hdy.2014.106 CrossRefPubMedGoogle Scholar
  37. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man 1871–1971. Heinemann, pp. 136–179Google Scholar
  38. Vala F, Egas M, Breeuwer JAJ, Sabelis MW (2004) Wolbachia affects oviposition and mating behaviour of its spider mite host. J Evol Biol 17:692–700. doi: 10.1046/j.1420-9101.2003.00679.x CrossRefPubMedGoogle Scholar
  39. Werren JH (1993) The evolution of inbreeding in haplodiploid organisms. In: Thornhill NW (ed) The natural history of inbreeding and outbreeding. Theoretical and empirical perspectives. The University of Chicago Press, Chicago, IL, pp 42–59Google Scholar
  40. Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751. doi: 10.1038/nrmicro1969 CrossRefPubMedGoogle Scholar
  41. Willis PM (2013) Why do animals hybridize? Acta Ethologica 16:127–134. doi: 10.1007/s10211-013-0144-6 CrossRefGoogle Scholar
  42. Wirtz P (1999) Mother species–father species: unidirectional hybridization in animals with female choice. Anim Behav 58:1–12. doi: 10.1006/anbe.1999.1144 CrossRefPubMedGoogle Scholar
  43. Yoshioka T, Yano S (2014) Do Tetranychus urticae males avoid mating with familiar females? J Exp Biol 217:2297–2300. doi: 10.1242/jeb.098277 CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Yukie Sato
    • 1
    • 2
  • Heike Staudacher
    • 1
  • Maurice W. Sabelis
    • 1
  1. 1.Institute for Biodiversity and Ecosystem DynamicsUniversity of AmsterdamAmsterdamThe Netherlands
  2. 2.Sugadaira Montane Research CenterUniversity of TsukubaUedaJapan

Personalised recommendations