Evolutionary Ecology

, Volume 31, Issue 5, pp 769–783 | Cite as

Avoidance of host resistance in the oviposition-site preferences of rose bitterling

  • Romain Rouchet
  • Carl Smith
  • Huanzhang Liu
  • Caroline Methling
  • Karel Douda
  • Dan Yu
  • Qionying Tang
  • Martin Reichard
Original Paper


A contemporary outcome of dynamic host–parasite coevolution can be driven by the adaptation of a parasite to exploit its hosts at the population and species levels (parasite specialisation) or by local host adaptations leading to greater host resistance to sympatric parasite populations (host resistance). We tested the predominance of these two scenarios using cross-infection experiments with two geographically distant populations of the rose bitterling, Rhodeus ocellatus, a fish brood parasite of freshwater mussels, and four populations of their mussel hosts (two Anodonta woodiana and two Unio douglasiae populations) with varying degrees of geographic sympatry and local coexistence. Our data support predictions for host resistance at the species level but no effect of local coexistence between specific populations. Rhodeus ocellatus showed a preference for allopatric host populations, irrespective of host species. Host mussel response, in terms of ejection of R. ocellatus eggs, was stronger in the more widespread and abundant host species (A. woodiana) and this response tended to be higher in sympatric populations. These outcomes provide support for the importance of host resistance in bitterling oviposition-site decisions, demonstrating that host choice by R. ocellatus is adaptive by minimizing egg ejections. These findings imply that R. ocellatus, and potentially other bitterling species, may benefit from exploiting novel hosts, which may not possess appropriate adaptive responses to parasitism.


Brood parasitism Coevolutionary dynamic Egg ejection Host selection Oviposition choice Parasite specialisation 



Funding came from the Czech Science Foundation (13-05872S). MR and CS designed the study. RR collected data with the help of HL, CM, KD, DY, and QT. CS, RR and MR analysed the data and RR, CS and MR drafted the ms, with contributions from HL and KD. We thank John Endler, Matt Hall and four anonymous referees for their constructive comments. Primary data associated with the paper are deposited at Figshare Repository (10.6084/m9.figshare.4797886).


  1. Adiba S, Huet M, Kaltz O (2010) Experimental evolution of local parasite maladaptation. J Evol Biol 23:1195–1205CrossRefPubMedGoogle Scholar
  2. Agbali M, Reichard M, Bryjová A, Bryja J, Smith C (2010) Mate choice for non-additive genetic benefits correlate with MHC dissimilarity in the rose bitterling (Rhodeus ocellatus). Evolution 64:1683–1696CrossRefPubMedGoogle Scholar
  3. Agbali M, Spence R, Reichard M, Smith C (2012) Direct fitness benefits are preferred when the strength of direct and indirect sexual selection are equivalent. Isr J Ecol Evol 58:279–288Google Scholar
  4. Aldridge DC (1999) Development of European bitterling in the gills of freshwater mussels. J Fish Biol 54:138–151CrossRefGoogle Scholar
  5. Auld SKJR, Penczykowski RM, Housley Ochs J, Grippi DC, Hall SR, Duffy MA (2013) Variation in costs of parasite resistance among natural host populations. J Evol Biol 26:2479–2486CrossRefPubMedGoogle Scholar
  6. Bartoń K (2014) MuMIn—multi-model inference (R package version 1.15.1). R Foundation for Statistical Computing, ViennaGoogle Scholar
  7. Bates D, Maechler M, Bolker B, Walker S, Christensen RHB, Singmann H, Dai B, Grothendieck G (2014) lme4: linear mixed-effects models using eigen and S4 (R package version 1.1–7). R Foundation for Statistical Computing, ViennaGoogle Scholar
  8. Casalini M, Agbali M, Reichard M, Konečná M, Bryjová A, Smith C (2009) Male dominance, female mate choice, and intersexual conflict in the rose bitterling (Rhodeus ocellatus). Evolution 63:366–376CrossRefPubMedGoogle Scholar
  9. Casalini M, Reichard M, Phillips Smith C (2013) Male choice of mates and mating resources in the rose bitterling (Rhodeus ocellatus). Behav Ecol 24:1119–1204CrossRefGoogle Scholar
  10. Chang CH et al (2014) Phylogenetic relationships of Acheilognathidae (Cypriniformes: Cyprinoidea) as revealed from evidence of both nuclear and mitochondrial gene sequence variation: evidence for necessary taxonomic revision in the family and the identification of cryptic species. Mol Phylogent Evol 81:182–194CrossRefGoogle Scholar
  11. Davies NB (2015) Cuckoo: cheating by nature. Bloomsbury, LondonGoogle Scholar
  12. Davies NB, Brooke ML (1988) Cuckoos versus reed warblers: adaptations and counteradaptations. Anim Behav 36:262–284CrossRefGoogle Scholar
  13. Dawkins R, Krebs JR (1979) Arms races between and within species. Proc R Soc B: Biol Sci 205:489–511Google Scholar
  14. Dillon RT (2000) The ecology of freshwater molluscs. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  15. Douda K, Vrtílek M, Slavík O, Reichard M (2012) The role of host specificity in explaining the invasion success of the freshwater mussel Anodonta woodiana in Europe. Biol Invasion 14:127–137CrossRefGoogle Scholar
  16. Edmunds GF, Alstad DN (1978) Coevolution in insect herbivores and conifers. Science 199:941–945CrossRefPubMedGoogle Scholar
  17. Font WF (2003) The global spread of parasites: what do Hawaiian streams tell us? Bioscience 53:1061–1067CrossRefGoogle Scholar
  18. Fox J et al (2016) Package ‘effects’ (R package version 3.1–2). R Foundation for Statistical Computing, ViennaGoogle Scholar
  19. Frankel VM, Hendry AP, Rolshausen G, Torchin ME (2015) Host preference of an introduced ‘generalist’ parasite for a non-native host. Int J Parasitol 45:703–709CrossRefPubMedGoogle Scholar
  20. Greischar MA, Koskella B (2007) A synthesis of experimental work on parasite local adaptation. Ecol Lett 10:418–434CrossRefPubMedGoogle Scholar
  21. Hanks LM, Denno RF (1994) Local adaptation in the armoured scale insect Pseudaulacaspis pentagona (Homoptera: Diaspididae). Ecology 75:2301–2310CrossRefGoogle Scholar
  22. Hasu T, Benesh DP, Valtonen ET (2009) Differences in parasite susceptibility and costs of resistance between naturally exposed and unexposed host populations. J Evol Biol 22:699–707CrossRefPubMedGoogle Scholar
  23. He J, Zimin Z (2013) The freshwater bivalves of China. ConchBooks, GermanyGoogle Scholar
  24. Hoeksema JD, Forde SE (2008) A meta-analysis of factors affecting local adaptation between interacting species. Am Nat 171:275–290CrossRefPubMedGoogle Scholar
  25. Holland JN, DeAngelis DL, Schultz ST (2004) Evolutionary stability of mutualism: interspecific population regulation as an evolutionary stable strategy. Proc R Soc Lond B 271:1807–1814CrossRefGoogle Scholar
  26. Honza M, Procházka P, Stokke BG, Mosknes A, Røskaft E, Čapek M, Mrlík V (2004) Are blackcaps current winners in the evolutionary struggle against the common cuckoo? J Ethol 22:175–180CrossRefGoogle Scholar
  27. Ieno EN, Zuur AF (2015) data exploration and visualisation with R. Highland Statistics Ltd, NewburghGoogle Scholar
  28. Joshi A, Thompson JN (1995) Trade-offs and the evolution of host specialization. Evol Ecol 9:82–92CrossRefGoogle Scholar
  29. Kaltz O, Shykoff JA (1998) Local adaptation in host–parasite systems. Heredity 81:361–370CrossRefGoogle Scholar
  30. Kawamura K, Ueda T, Arai R, Nagata Y, Saitoh K, Ohtaka H, Kanoh Y (2001) Genetic introgression by the rose bitterling, Rhodeus ocellatus ocellatus, into the Japanese rose bitterling, R. o. kurumeus (Teleostei: Cyprinidae). Zool Sci 18:1027–1039CrossRefGoogle Scholar
  31. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241CrossRefGoogle Scholar
  32. Kelehear C, Saltonstall K, Torchin MM (2015) An introduced parasite (Raillietiella frenata) infects native cane toads (Rhinella marina) in Panama. Parasitol 142:675–679CrossRefGoogle Scholar
  33. Kitamura J (2005) Factors affecting seasonal mortality of rosy bitterling (Rhodeus ocellatus kurumeus) embryos on the gills of their host mussel. Popul Ecol 47:41–51CrossRefGoogle Scholar
  34. Krasnov BR, Poulin R, Mouillot D (2011) Scale-dependence of phylogenetic signal in ecological traits of ectoparasites. Ecography 34:114–122CrossRefGoogle Scholar
  35. Kuehn MJ (2009) Persistence versus decline of host defences against brood parasitism: a model system for studies of relaxed selection and phenotypic plasticity? Ph.D. thesis, University of California, Santa BarbaraGoogle Scholar
  36. Laine AL (2009) Role of coevolution in generating biological diversity: spatially divergent selection trajectories. J Exp Bot 60:2957–2970CrossRefPubMedGoogle Scholar
  37. Lajeunesse MJ, Forbes MR (2002) Host range and local parasite adaptation. Proc R Soc Lond B 269:703–710CrossRefGoogle Scholar
  38. Liu H, Zhu Y, Smith C, Reichard M (2006) Evidence of host specificity and congruence between phylogenies of bitterlings and freshwater mussels. Zool Stud 45:428–434Google Scholar
  39. Lively CM, Jokela J (1996) Clinal variation for local adaptation in a host–parasite interaction. Proc R Soc Lond B 263:891–897CrossRefGoogle Scholar
  40. Medina I, Langmore NE (2016) The evolution of host specialisation in avian brood parasites. Ecol Lett 19:1110–1118CrossRefPubMedGoogle Scholar
  41. Mills SC, Reynolds JD (2002) Mussel ventilation rates as a proximate cue for host selection by bitterling, Rhodeus sericeus. Oecologia 131:473–478CrossRefPubMedGoogle Scholar
  42. Moret Y, Schmid-Hempel P (2000) Survival for immunity: the price of immune system activation for bumblebee workers. Science 290:1166–1168CrossRefPubMedGoogle Scholar
  43. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Method Ecol Evol 4:133–142CrossRefGoogle Scholar
  44. Pateman-Jones C, Rasotto MB, Reichard M, Liao C, Liu HZ, Zięba G, Smith C (2011) Variation in male reproductive traits among three bitterling fishes (Acheilognathinae: Cyprinidae) in relation to the mating system. Biol J Linn Soc 103:622–632CrossRefGoogle Scholar
  45. Phillips A, Reichard M, Smith C (2017) Sex differences in the oviposition-site decisions of a fish. Anim Behav (accepted)Google Scholar
  46. R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  47. Reichard M, Jurajda P, Smith C (2004a) Male-male interference competition decreases spawning rate in the European bitterling (Rhodeus sericeus). Behav Ecol Sociobiol 56:34–41CrossRefGoogle Scholar
  48. Reichard M, Smith C, Jordan WC (2004b) Genetic evidence reveals density-dependent mediated success of alternative mating tactics in the European bitterling (Rhodeus sericeus). Mol Ecol 13:1569–1578CrossRefPubMedGoogle Scholar
  49. Reichard M, Ondračková M, Przybylski M, Liu HZ, Smith C (2006) The costs and benefits in an unusual symbiosis: experimental evidence that bitterling fish (Rhodeus sericeus) are parasites of unionid mussels in Europe. J Evol Biol 19:788–796CrossRefPubMedGoogle Scholar
  50. Reichard M, Liu H, Smith C (2007a) The co-evolutionary relationship between bitterling fishes and freshwater mussels: insights from interspecific comparisons. Evol Ecol Res 9:1–21Google Scholar
  51. Reichard M, Przybylski M, Kaniewska P, Liu H, Smith C (2007b) A possible evolutionary lag in the relationship between freshwater mussels and European bitterling. J Fish Biol 70:709–725CrossRefGoogle Scholar
  52. Reichard M, Polačik M, Tarkan AS, Spence R, Gaygusuz Ö, Ercan E, Ondračková M, Smith C (2010) The bitterling–mussel coevolutionary relationship in areas of recent and ancient sympatry. Evolution 64:3047–3056PubMedGoogle Scholar
  53. Reichard M, Bryja J, Polačik M, Smith C (2011) No evidence for host specialization or host-race formation in the European bitterling (Rhodeus amarus), a fish that parasitizes freshwater mussels. Mol Ecol 20:3631–3643PubMedGoogle Scholar
  54. Reichard M, Vrtílek M, Douda K, Smith C (2012) An invasive species reverses the roles in a host–parasite relationship between fish and unionid mussels. Biol Lett 8:601–604CrossRefPubMedPubMedCentralGoogle Scholar
  55. Reichard M, Douda K, Przybyłski M, Popa OP, Karbanová E, Matasová K et al (2015) Population-specific responses to an invasive species. Proc R Soc Lond B 282:20151063CrossRefGoogle Scholar
  56. Rigby M, Moret Y (2000) Life-history trade-offs with immune defenses. In: Poulin R, Morand S, Skorping A (eds) Evolutionary biology of host–parasite relationships: theory meets reality. Elsevier, Amsterdam, pp 129–142Google Scholar
  57. Rothstein SI, Robinson SK (1998) Parasitic birds and their hosts. Studies in coevolution. Oxford University Press, OxfordGoogle Scholar
  58. Schmid-Hempel P (2003) Variation in immune defence as a question of evolutionary ecology. Proc R Soc Lond B 270:357–366CrossRefGoogle Scholar
  59. Smith C (2017) Bayesian inference supports the host selection hypothesis in explaining adaptive host specificity by European bitterling. Oecologia 183:379–389CrossRefPubMedGoogle Scholar
  60. Smith C, Reichard M (2013) A sperm competition model for the European bitterling (Rhodeus amarus). Behaviour 150:1709–1730CrossRefGoogle Scholar
  61. Smith C, Rippon K, Douglas A, Jurajda P (2001) A proximate cue for oviposition site choice in the bitterling (Rhodeus sericeus). Freshw Biol 46:903–911CrossRefGoogle Scholar
  62. Smith C, Reichard M, Jurajda P (2003) Assessment of sperm competition by European bitterling, Rhodeus sericeus. Behav Ecol Sociobiol 53:206–213CrossRefGoogle Scholar
  63. Smith C, Reichard M, Jurajda P et al (2004) The reproductive ecology of the European bitterling (Rhodeus sericeus). J Zool Lond 262:107–124CrossRefGoogle Scholar
  64. Sorenson MD, Sefc KM, Payne RB (2003) Speciation by host switch in brood parasitic indigobirds. Nature 424:928–931CrossRefPubMedGoogle Scholar
  65. Spence R, Smith C (2013) Rose bitterling (Rhodeus ocellatus) embryos parasitise freshwater mussels by competing for nutrients and oxygen. Acta Zool 94:113–118CrossRefGoogle Scholar
  66. Thompson JN (1994) The Coevolutionary Process. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  67. Thompson JN (1999) The raw material for coevolution. Oikos 84:5–16CrossRefGoogle Scholar
  68. Thompson JN (2013) Relentless evolution. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  69. Vasil’eva ED, Mamilov NS, Magda IN (2015) New species of Cypriniform fishes (Cypriniformes) in the fauna of the Balkhash-Ili basin, Kazhakhstan. J Ichthyol 55:447–453CrossRefGoogle Scholar
  70. Voutilainen A, Valdez H, Karvonen A, Kortet R, Kuukka H, Peuhkuri N, Piironen J, Taskinen J (2009) Infectivity of trematode eye flukes in farmed salmonid fish—effects of parasite and host origins. Aquaculture 293:108–112CrossRefGoogle Scholar
  71. Watters GT (1997) A synthesis and review of the expanding range of the Asian freshwater mussel Anodonta woodiana (Lea, 1834) (Bivalvia, Unionidae). Veliger 40:152–156Google Scholar
  72. Welcomme RL (1988) International introductions of inland aquatic species. FAO Fish Tech Pap 294:318Google Scholar
  73. Woolhouse ME, Webster JP, Domingo E, Charlesworth B, Levin BR (2002) Biological and biomedical applications of the co-evolution of pathogens and their hosts. Nat Genet 32:569–577CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  1. 1.Institute of Vertebrate BiologyAcademy of Sciences of the Czech RepublicBrnoCzech Republic
  2. 2.School of BiologyUniversity of St AndrewsSt AndrewsUK
  3. 3.Bell-Pettigrew Museum of Natural HistoryUniversity of St AndrewsSt AndrewsUK
  4. 4.The Key Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences, Institute of HydrobiologyChinese Academy of SciencesWuhanPeople’s Republic of China
  5. 5.Department of Zoology and Fisheries, Faculty of Agrobiology Food and Natural ResourcesCzech University of Life Sciences PraguePragueCzech Republic

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