Abstract
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.
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References
Adiba S, Huet M, Kaltz O (2010) Experimental evolution of local parasite maladaptation. J Evol Biol 23:1195–1205
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 64:1683–1696
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 58:279–288
Aldridge DC (1999) Development of European bitterling in the gills of freshwater mussels. J Fish Biol 54:138–151
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 26:2479–2486
Bartoń K (2014) MuMIn—multi-model inference (R package version 1.15.1). R Foundation for Statistical Computing, Vienna
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, Vienna
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 63:366–376
Casalini M, Reichard M, Phillips Smith C (2013) Male choice of mates and mating resources in the rose bitterling (Rhodeus ocellatus). Behav Ecol 24:1119–1204
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 81:182–194
Davies NB (2015) Cuckoo: cheating by nature. Bloomsbury, London
Davies NB, Brooke ML (1988) Cuckoos versus reed warblers: adaptations and counteradaptations. Anim Behav 36:262–284
Dawkins R, Krebs JR (1979) Arms races between and within species. Proc R Soc B: Biol Sci 205:489–511
Dillon RT (2000) The ecology of freshwater molluscs. Cambridge University Press, Cambridge
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 14:127–137
Edmunds GF, Alstad DN (1978) Coevolution in insect herbivores and conifers. Science 199:941–945
Font WF (2003) The global spread of parasites: what do Hawaiian streams tell us? Bioscience 53:1061–1067
Fox J et al (2016) Package ‘effects’ (R package version 3.1–2). R Foundation for Statistical Computing, Vienna
Frankel VM, Hendry AP, Rolshausen G, Torchin ME (2015) Host preference of an introduced ‘generalist’ parasite for a non-native host. Int J Parasitol 45:703–709
Greischar MA, Koskella B (2007) A synthesis of experimental work on parasite local adaptation. Ecol Lett 10:418–434
Hanks LM, Denno RF (1994) Local adaptation in the armoured scale insect Pseudaulacaspis pentagona (Homoptera: Diaspididae). Ecology 75:2301–2310
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 22:699–707
He J, Zimin Z (2013) The freshwater bivalves of China. ConchBooks, Germany
Hoeksema JD, Forde SE (2008) A meta-analysis of factors affecting local adaptation between interacting species. Am Nat 171:275–290
Holland JN, DeAngelis DL, Schultz ST (2004) Evolutionary stability of mutualism: interspecific population regulation as an evolutionary stable strategy. Proc R Soc Lond B 271:1807–1814
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 22:175–180
Ieno EN, Zuur AF (2015) data exploration and visualisation with R. Highland Statistics Ltd, Newburgh
Joshi A, Thompson JN (1995) Trade-offs and the evolution of host specialization. Evol Ecol 9:82–92
Kaltz O, Shykoff JA (1998) Local adaptation in host–parasite systems. Heredity 81:361–370
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 18:1027–1039
Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241
Kelehear C, Saltonstall K, Torchin MM (2015) An introduced parasite (Raillietiella frenata) infects native cane toads (Rhinella marina) in Panama. Parasitol 142:675–679
Kitamura J (2005) Factors affecting seasonal mortality of rosy bitterling (Rhodeus ocellatus kurumeus) embryos on the gills of their host mussel. Popul Ecol 47:41–51
Krasnov BR, Poulin R, Mouillot D (2011) Scale-dependence of phylogenetic signal in ecological traits of ectoparasites. Ecography 34:114–122
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 Barbara
Laine AL (2009) Role of coevolution in generating biological diversity: spatially divergent selection trajectories. J Exp Bot 60:2957–2970
Lajeunesse MJ, Forbes MR (2002) Host range and local parasite adaptation. Proc R Soc Lond B 269:703–710
Liu H, Zhu Y, Smith C, Reichard M (2006) Evidence of host specificity and congruence between phylogenies of bitterlings and freshwater mussels. Zool Stud 45:428–434
Lively CM, Jokela J (1996) Clinal variation for local adaptation in a host–parasite interaction. Proc R Soc Lond B 263:891–897
Medina I, Langmore NE (2016) The evolution of host specialisation in avian brood parasites. Ecol Lett 19:1110–1118
Mills SC, Reynolds JD (2002) Mussel ventilation rates as a proximate cue for host selection by bitterling, Rhodeus sericeus. Oecologia 131:473–478
Moret Y, Schmid-Hempel P (2000) Survival for immunity: the price of immune system activation for bumblebee workers. Science 290:1166–1168
Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Method Ecol Evol 4:133–142
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 103:622–632
Phillips A, Reichard M, Smith C (2017) Sex differences in the oviposition-site decisions of a fish. Anim Behav (accepted)
R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Reichard M, Jurajda P, Smith C (2004a) Male-male interference competition decreases spawning rate in the European bitterling (Rhodeus sericeus). Behav Ecol Sociobiol 56:34–41
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 13:1569–1578
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 19:788–796
Reichard M, Liu H, Smith C (2007a) The co-evolutionary relationship between bitterling fishes and freshwater mussels: insights from interspecific comparisons. Evol Ecol Res 9:1–21
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 70:709–725
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 64:3047–3056
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 20:3631–3643
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 8:601–604
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 282:20151063
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 129–142
Rothstein SI, Robinson SK (1998) Parasitic birds and their hosts. Studies in coevolution. Oxford University Press, Oxford
Schmid-Hempel P (2003) Variation in immune defence as a question of evolutionary ecology. Proc R Soc Lond B 270:357–366
Smith C (2017) Bayesian inference supports the host selection hypothesis in explaining adaptive host specificity by European bitterling. Oecologia 183:379–389
Smith C, Reichard M (2013) A sperm competition model for the European bitterling (Rhodeus amarus). Behaviour 150:1709–1730
Smith C, Rippon K, Douglas A, Jurajda P (2001) A proximate cue for oviposition site choice in the bitterling (Rhodeus sericeus). Freshw Biol 46:903–911
Smith C, Reichard M, Jurajda P (2003) Assessment of sperm competition by European bitterling, Rhodeus sericeus. Behav Ecol Sociobiol 53:206–213
Smith C, Reichard M, Jurajda P et al (2004) The reproductive ecology of the European bitterling (Rhodeus sericeus). J Zool Lond 262:107–124
Sorenson MD, Sefc KM, Payne RB (2003) Speciation by host switch in brood parasitic indigobirds. Nature 424:928–931
Spence R, Smith C (2013) Rose bitterling (Rhodeus ocellatus) embryos parasitise freshwater mussels by competing for nutrients and oxygen. Acta Zool 94:113–118
Thompson JN (1994) The Coevolutionary Process. University of Chicago Press, Chicago
Thompson JN (1999) The raw material for coevolution. Oikos 84:5–16
Thompson JN (2013) Relentless evolution. University of Chicago Press, Chicago
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 55:447–453
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 293:108–112
Watters GT (1997) A synthesis and review of the expanding range of the Asian freshwater mussel Anodonta woodiana (Lea, 1834) (Bivalvia, Unionidae). Veliger 40:152–156
Welcomme RL (1988) International introductions of inland aquatic species. FAO Fish Tech Pap 294:318
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 32:569–577
Acknowledgements
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).
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Rouchet, R., Smith, C., Liu, H. et al. Avoidance of host resistance in the oviposition-site preferences of rose bitterling. Evol Ecol 31, 769–783 (2017). https://doi.org/10.1007/s10682-017-9907-2
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DOI: https://doi.org/10.1007/s10682-017-9907-2