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Autonomy and integration in complex parasite life cycles

Published online by Cambridge University Press:  29 September 2016

DANIEL P. BENESH
DANIEL P. BENESH*
Affiliation:
Marine Science Institute, University of California, Santa Barbara, CA 93106-6150, USA
*
*Corresponding author: Marine Science Institute, University of California, Santa Barbara, CA 93106-6150, USA. E-mail: [email protected]
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Summary

Complex life cycles are common in free-living and parasitic organisms alike. The adaptive decoupling hypothesis postulates that separate life cycle stages have a degree of developmental and genetic autonomy, allowing them to be independently optimized for dissimilar, competing tasks. That is, complex life cycles evolved to facilitate functional specialization. Here, I review the connections between the different stages in parasite life cycles. I first examine evolutionary connections between life stages, such as the genetic coupling of parasite performance in consecutive hosts, the interspecific correlations between traits expressed in different hosts, and the developmental and functional obstacles to stage loss. Then, I evaluate how environmental factors link life stages through carryover effects, where stressful larval conditions impact parasites even after transmission to a new host. There is evidence for both autonomy and integration across stages, so the relevant question becomes how integrated are parasite life cycles and through what mechanisms? By highlighting how genetics, development, selection and the environment can lead to interdependencies among successive life stages, I wish to promote a holistic approach to studying complex life cycle parasites and emphasize that what happens in one stage is potentially highly relevant for later stages.

Keywords

body sizegrowthdevelopmentmetamorphosisoverhead costsparental effectssimple life cyclequantitative geneticslife historyphylogenetic regression
Type
Review Article
Information
Parasitology , Volume 143 , Issue 14 , December 2016 , pp. 1824 - 1846
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Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Abrams, P. and Rowe, L. (1996). The effects of predation on the age and size of maturity of prey. Evolution 50, 1052–1061.Google Scholar
Abrams, P., Leimar, O., Nylin, S. and Wiklund, C. (1996). The effect of flexible growth rates on optimal sizes and development times in a seasonal environment. American Naturalist 147, 381–395.Google Scholar
Aguirre, J., Blows, M. W. and Marshall, D. J. (2014). The genetic covariance between life cycle stages separated by metamorphosis. Proceedings of the Royal Society B: Biological Sciences 281, 20141091.Google Scholar
Alto, B. W., Lounibos, L. P., Higgs, S. and Juliano, S. A. (2005). Larval competition differentially affects arbovirus infection in Aedes mosquitoes. Ecology 86, 3279–3288.CrossRefGoogle ScholarPubMed
Álvarez, D. and Nicieza, A. G. (2002). Effects of induced variation in anuran larval development on postmetamorphic energy reserves and locomotion. Oecologia 131, 186–195.Google Scholar
Anderson, R. (1988). Nematode transmission patterns. Journal of Parasitology 74, 30–45.CrossRefGoogle ScholarPubMed
Andreassen, J., Ito, A., Ito, M., Nakao, M. and Nakaya, K. (2004). Hymenolepis microstoma: direct life cycle in immunodeficient mice. Journal of Helminthology 78, 1–5.Google Scholar
Angilletta, M., Steury, T. D. and Sears, M. W. (2004). Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integrative and Comparative Biology 44, 498–509.Google Scholar
Appy, R. G. and Butterworth, E. W. (2011). Development of Ascarophis sp. (Nematoda: Cystidicolidae) to maturity in Gammarus deubeni (Amphipoda). Journal of Parasitology 97, 1035–1048.Google Scholar
Arbeitman, M. N., Furlong, E. E. M., Imam, F., Johnson, E., Null, B. H., Baker, B. S., Krasnow, M. A, Scott, M. P., Davis, R. W. and White, K. P. (2002). Gene expression during the life cycle of Drosophila melanogaster . Science 297, 2270–2275..Google Scholar
Archer, D. and Hopkins, C. (1958). Studies on cestode metabolism. V. The chemical composition of Diphyllobothrium sp. in the plerocercoid and adult stages. Experimental Parasitology 554, 542–554.Google Scholar
Arendt, J. D. (2011). Size-fecundity relationships, growth trajectories, and the temperature-size rule for ectotherms. Evolution 65, 43–51.Google Scholar
Arene, F. O. I. (1986). Ascaris suum: influence of embryonation temperature on the viability of the infective larva. Journal of Thermal Biology 11, 9–15.CrossRefGoogle Scholar
Arneberg, P., Skorping, A. and Read, A. F. (1998). Parasite abundance, body size, life histories, and the energetic equivalence rule. American Naturalist 151, 497–513.Google Scholar
Atkinson, D. (1994). Temperature and organism size-a biological law for ectotherms? Advances in Ecological Research 25, 1–58.CrossRefGoogle Scholar
Auld, S. K. J. R. and Tinsley, M. C. (2015). The evolutionary ecology of complex lifecycle parasites: linking phenomena with mechanisms. Heredity 114, 125–132.Google Scholar
Ball, M. A., Parker, G. A. and Chubb, J. C. (2008). The evolution of complex life cycles when parasite mortality is size- or time-dependent. Journal of Theoretical Biology 253, 202–214.Google Scholar
Barber, I. (2005). Parasites grow larger in faster growing fish hosts. International Journal for Parasitology 35, 137–143.Google Scholar
Baron, R. W. and Tanner, C. E. (1976). The effect of immunosuppression on secondary Echinococcus multilocularis infections in mice. International Journal for Parasitology 6, 37–42.CrossRefGoogle ScholarPubMed
Bartlett, C. M. (1996). Morphogenesis of Contracaecum rudolphii (Nematoda: Ascaridoidea), a parasite of fish-eating birds, in its copepod precursor and fish intermediate hosts. Parasite 4, 367–376.Google Scholar
Baum, J., Gilberger, T.-W., Frischknecht, F. and Meissner, M. (2008). Host-cell invasion by malaria parasites: insights from Plasmodium and Toxoplasma . Trends in Parasitology 24, 557–563.Google Scholar
Bellay, S., de Oliveira, E. F., Almeida-Neto, M., Lima Junior, D. P., Takemoto, R. M. and Luque, J. L. (2013). Developmental stage of parasites influences the structure of fish-parasite networks. PLoS ONE 8, e75710.Google Scholar
Benesh, D. P. (2010). Developmental inflexibility of larval tapeworms in response to resource variation. International Journal for Parasitology 40, 487–497.CrossRefGoogle ScholarPubMed
Benesh, D. P. (2011). Intensity-dependent host mortality: what can it tell us about larval growth strategies in complex life cycle helminths? Parasitology 138, 913–925.Google Scholar
Benesh, D. P. and Hafer, N. (2012). Growth and ontogeny of the tapeworm Schistocephalus solidus in its copepod first host affects performance in its stickleback second intermediate host. Parasites & Vectors 5, 90.Google Scholar
Benesh, D. P. and Valtonen, E. T. (2007 a). Sexual differences in larval life history traits of acanthocephalan cystacanths. International Journal for Parasitology 37, 191–198.Google Scholar
Benesh, D. P. and Valtonen, E. T. (2007 b). Proximate factors affecting the larval life history of Acanthocephalus lucii (Acanthocephala). Journal of Parasitology 93, 742–749.Google Scholar
Benesh, D. P., Chubb, J. C. and Parker, G. A. (2011). Exploitation of the same trophic link favors convergence of larval life-history strategies in complex life cycle helminths. Evolution 65, 2286–2299.Google Scholar
Benesh, D. P., Weinreich, F. and Kalbe, M. (2012). The relationship between larval size and fitness in the tapeworm Schistocephalus solidus: bigger is better? Oikos 121, 1391–1399.Google Scholar
Benesh, D. P., Chubb, J. C. and Parker, G. A. (2013). Complex life cycles: why refrain from growth before reproduction in the adult niche? American Naturalist 181, 39–51.Google Scholar
Benesh, D. P., Chubb, J. C. and Parker, G. A. (2014 a). The trophic vacuum and the evolution of complex life cycles in trophically transmitted helminths. Proceedings of the Royal Society B: Biological Sciences 281, 20141462.Google Scholar
Benesh, D. P., Weinreich, F., Kalbe, M. and Milinski, M. (2014 b). Lifetime inbreeding depression, purging, and mating system evolution in a simultaneous hermaphrodite tapeworm. Evolution 68, 1762–1774.Google Scholar
Berntzen, A. K. and Mueller, J. F. (1964). In vitro cultivation of Spirometra mansonoides (Cestoda) from the procercoid to the early adult. Journal of Parasitology 50, 705–711.Google Scholar
Bersier, L. F. and Kehrli, P. (2008). The signature of phylogenetic constraints on food-web structure. Ecological Complexity 5, 132–139.Google Scholar
Blows, M. and Hoffmann, A. (2005). A reassessment of genetic limits to evolutionary change. Ecology 86, 1371–1384.CrossRefGoogle Scholar
Bouchard, S. S., Leary, C. J. O., Wargelin, L. J., Charbonnier, J. F. and Warkentin, K. M. (2016). Post-metamorphic carry-over effects of larval digestive plasticity. Functional Ecology 30, 379–388.Google Scholar
Brandt, F. H. and Eberhard, M. L. (1990). Dracunculus insignis in ferrets: comparison of inoculation routes. Journal of Parasitology 76, 93–95.Google Scholar
Brittain, J. E. (1982). Biology of mayflies. Annual Review of Entomology 27, 119–147.CrossRefGoogle Scholar
Brodin, T. (2009). Behavioral syndrome over the boundaries of life — carryovers from larvae to adult damselfly. Behavioral Ecology 20, 30–37.Google Scholar
Brose, U., Jonsson, T., Berlow, E. L., Warren, P., Banasek-Richter, C., Bersier, L. F., Blanchard, J. L., Brey, T., Carpenter, S. R., Blandenier, M. F. C., Cushing, L., Dawah, H. A., Dell, T., Edwards, F., Harper-Smith, S., Jacob, U., Ledger, M. E., Martinez, N. D., Memmott, J., Mintenbeck, K., Pinnegar, J. K., Rall, B. C., Rayner, T. S., Reuman, D. C., Ruess, L., Ulrich, W., Williams, R. J., Woodward, G. and Cohen, J. E. (2006). Consumer-resource body-size relationships in natural food webs. Ecology 87, 2411–2417.Google Scholar
Brown, S. P., Renaud, F., Guegan, J.-F. and Thomas, F. (2001). Evolution of trophic transmission in parasites: the need to reach a mating place? Journal of Evolutionary Biology 14, 815–820.Google Scholar
Brown, S. P., De Lorgeril, J., Joly, C. and Thomas, F. (2003). Field evidence for density-dependent effects in the trematode Microphallus papillorobustus in its manipulated host, Gammarus insensibilis . Journal of Parasitology 89, 668–672.Google Scholar
Brown, J., Gillooly, J., Allen, A., Savage, V. and West, G. (2004). Toward a metabolic theory of ecology. Ecology 85, 1771–1789.Google Scholar
Bryan, P. J. (2004). Energetic cost of development through metamorphosis for the seastar Mediaster aequalis (Stimpson). Marine Biology 145, 293–302.Google Scholar
Calentine, R. L. (1964). Life cycle of Archigetes iowensis (Cestoda – Caryophyllaeidae). Journal of Parasitology 50, 454–458.Google Scholar
Callery, E. M., Fang, H. and Elinson, R. P. (2001). Frogs without polliwogs: evolution of anuran direct development. BioEssays 23, 233–241.Google Scholar
Cartwright, P. and Nawrocki, A. M. (2010). Character evolution in Hydrozoa (phylum Cnidaria). Integrative and Comparative Biology 50, 456–472.Google Scholar
Casanova, J. C., Santalla, F., Durand, P., Vaucher, C., Feliu, C. and Renaud, F. (2001). Morphological and genetic differentiation of Rodentolepis straminea (Goeze, 1752) and Rodentolepis microstoma (Dujardin, 1845) (Hymenolepididae). Parasitology Research 87, 439–444.Google Scholar
Chandler, A., Read, C. and Nicholas, H. (1950). Observations on certain phases of nutrition and host-parasite relations of Hymenolepis diminuta in white rats. Journal of Parasitology 36, 523–535.Google Scholar
Chippindale, A. K., Chu, T. J. F. and Rose, M. R. (1996). Complex trade-offs and the evolution of starvation resistance in Drosophila melanogaster . Evolution 50, 753–766.Google Scholar
Choisy, M., Brown, S. P., Lafferty, K. D. and Thomas, F. (2003). Evolution of trophic transmission in parasites: why add intermediate hosts? American Naturalist 162, 172–181.CrossRefGoogle ScholarPubMed
Chubb, J. C., Ball, M. A. and Parker, G. A. (2010). Living in intermediate hosts: evolutionary adaptations in larval helminths. Trends in Parasitology 26, 93–102.Google Scholar
Colinet, H., Boivin, G. and Hance, T. (2007). Manipulation of parasitoid size using the temperature-size rule: fitness consequences. Oecologia 152, 425–433.Google Scholar
Collins, A. G. (2002). Phylogeny of Medosozoa and the evolution of the cnidarian life cycles. Journal of Evolutionary Biology 15, 418–432.Google Scholar
Collins, A. G., Bentlage, B., Lindner, A., Lindsay, D., Haddock, S. H. D., Jarms, G., Norenburg, J. L., Jankowski, T. and Cartwright, P. (2008). Phylogenetics of Trachylina (Cnidaria: Hydrozoa) with new insights on the evolution of some problematical taxa. Journal of the Marine Biological Association of the United Kingdom 88, 1673.CrossRefGoogle Scholar
Cooper, C. L., Crites, J. L. and Sprinkle-Fastkie, D. J. (1978). Population biology and behavior of larval Eustrongylides tubifex (Nematoda: Dioctophymatida) in poikilothermous hosts. Journal of Parasitology 64, 102–107.Google Scholar
Corkum, K. C. and Beckerdite, F. W. (1975). Observations on the life history of Alloglossidium macrobdellensis (Trematoda: Macroderoididae) from Macrobdella ditetra (Hirudinea: Hirudinidae). American Midland Naturalist 93, 484–491.CrossRefGoogle Scholar
Coyner, D. F., Spalding, M. G. and Forrester, D. J. (2003). Epizootiology of Eustrongylides ignotus in Florida: transmission and development of larvae in intermediate hosts. Journal of Parasitology 89, 290–298.CrossRefGoogle ScholarPubMed
Crean, A. J., Monro, K. and Marshall, D. J. (2011). Fitness consequences of larval traits persist across the metamorphic boundary. Evolution 65, 3079–3089.CrossRefGoogle ScholarPubMed
Cribb, T. H., Bray, R. A. and Littlewood, D. T. J. (2001). The nature and evolution of the association among digeneans, molluscs and fishes. International Journal for Parasitology 31, 997–1011.Google Scholar
Crichton, V. F. J. and Beverley-Burton, M. (1975). Migration, growth and morphogenesis of Dracunculus insignis (Nematoda dracunculoidea). Canadian Journal of Zoology 53, 105–113.Google Scholar
Crichton, V. F. J. and Beverley-Burton, M. (1977). Observations on the seasonal prevalence, pathology and transmission of Dracunculus insignis (Nematoda: Dracunculoidea) in the raccoon (Procyon lotor L.) in Ontario. Journal of Wildlife Diseases 13, 273–280.Google Scholar
Crompton, D. W. T. (1985). Reproduction. In Biology of the Acanthocephala (ed. Crompton, D. , W. T. and Nickol, B. B.), pp. 213–272. Cambridge University Press, Cambridge.Google Scholar
Crompton, D. W. T. and Nickol, B. B. (1985). Biology of the Acanthocephala. Cambridge University Press, Cambridge.Google Scholar
Cwiklinski, K., Dalton, J. P., Dufresne, P. J., La Course, J., Williams, D. J. L., Hodgkinson, J. and Paterson, S. (2015). The Fasciola hepatica genome: gene duplication and polymorphism reveals adaptation to the host environment and the capacity for rapid evolution. Genome Biology 16, 71.Google Scholar
Daniels, R. R., Beltran, S., Poulin, R. and Lagrue, C. (2013). Do parasites adopt different strategies in different intermediate hosts? Host size, not host species, influences Coitocaecum parvum (Trematoda) life history strategy, size and egg production. Parasitology 140, 275–283.Google Scholar
Davies, S. J. and McKerrow, J. H. (2003). Developmental plasticity in schistosomes and other helminths. International Journal for Parasitology 33, 1277–1284.CrossRefGoogle ScholarPubMed
Davies, C. M., Webster, J. P., Woolhous, M. E. and Woolhouse, M. E. J. (2001). Trade-offs in the evolution of virulence in an indirectly transmitted macroparasite. Proceedings of the Royal Society B: Biological Sciences 268, 251–257.Google Scholar
Day, T. and Rowe, L. (2002). Developmental thresholds and the evolution of reaction norms for age and size at life-history transitions. American Naturalist 159, 338–350.Google Scholar
De Block, M. and Stoks, R. (2005). Fitness effects from egg to reproduction: bridging the life history transition. Ecology 86, 185–197.Google Scholar
De Rycke, P. H. and Berntzen, A. K. (1967). Maintenance and growth of Hymenolepis microstoma (Cestoda: Cyclophyllidea) in vitro . Journal of Parasitology 53, 352–354.Google Scholar
Dell, A. I., Pawar, S. and Savage, V. M. (2011). Systematic variation in the temperature dependence of physiological and ecological traits. Proceedings of the National Academy of Sciences of the United States of America 108, 10591–10596.Google Scholar
Denlinger, D. L. and Ma, W.-C. (1974). Dynamics of the pregnancy cycle in the tsetse Glossina morsitans . Journal of Insect Physiology 20, 1015–1026.Google Scholar
Denver, R. J. and Middlemis-Maher, J. (2010). Lessons from evolution: developmental plasticity in vertebrates with complex life cycles. Journal of Developmental Origins of Health and Disease 1, 282–291.Google Scholar
Dezfuli, B. S., Giari, L. and Poulin, R. (2001). Costs of intraspecific and interspecific host sharing in acanthocephalan cystacanths. Parasitology 122, 483–489.CrossRefGoogle ScholarPubMed
Dobson, A. P. (1986). Inequalities in the individual reproductive success of parasites. Parasitology 92, 675–682.Google Scholar
Dörücü, M., Wilson, D. and Barber, I. (2007). Differences in adult egg output of Schistocephalus solidus from singly-and multiply-infected sticklebacks. Journal of Parasitology 93, 1518–1520.Google Scholar
Dubey, J. P. (2006). Comparative infectivity of oocysts and bradyzoites of Toxoplasma gondii for intermediate (mice) and definitive (cats) hosts. Veterinary Parasitology 140, 69–75.Google Scholar
Dubinina, M. N. (1980). Tapeworms (Cestoda, Ligulidae) of the Fauna of the USSR. Amerind Publishing Co. Pvt. Ltd., New Dehli.Google Scholar
Dunsmore, J. D. and Spratt, D. M. (1979). The life history of Filaroides olseri in wild and domestic canids in Australia. Veterinary Parasitology 5, 275–286.Google Scholar
Dvorak, J., Jones, A. and Kuhlman, H. (1961). Studies on the biology of Hymenolepis microstoma (Dujardin, 1845). Journal of Parasitology 47, 833–838.Google Scholar
Dziekońska-Rynko, J., Rokicki, J. and Gomułka, P. (2010). Development of larval Contracaecum rudolphii Hartwich, 1964 (Ascaridida: Anisakidae) in experimentally infected goldfish (Carassius auratus L., 1758). Journal of Helminthology 84, 234–240.Google Scholar
Ebenman, B. (1992). Evolution in organisms that change their niches during the life-cycle. American Naturalist 139, 990–1021.Google Scholar
Elinson, R. P. and del Pino, E. M. (2012). Developmental diversity of amphibians. Wiley Interdisciplinary Reviews: Developmental Biology 1, 345–369.Google Scholar
Espinoza, I., Galindo, M., Bizarro, C. V., Ferreira, H. B., Zaha, A. and Galanti, N. (2005). Early post-larval development of the endoparasitic platyhelminth Mesocestoides corti: trypsin provokes reversible tegumental damage leading to serum-induced cell proliferation and growth. Journal of Cellular Physiology 205, 211–217.Google Scholar
Evans, N. A. (1985). The influence of environmental temperature upon transmission of the cercariae of Echinostoma liei (Digenea: Echinostomatidae). Parasitology 90, 269–275.Google Scholar
Fellous, S. and Lazzaro, B. P. (2011). Potential for evolutionary coupling and decoupling of larval and adult immune gene expression. Molecular Ecology 20, 1558–1567.Google Scholar
Ferguson, H. M., Mackinnon, M. J., Chan, B. H. and Read, A. F. (2003). Mosquito mortality and the evolution of malaria virulence. Evolution 57, 2792–2804.Google Scholar
Fisher, R. A. (1941). Average excess and average effect of a gene substitution. Annals of Eugenics 11, 53–63.CrossRefGoogle Scholar
Forster, J., Hirst, A. G. and Woodward, G. (2011). Growth and development rates have different thermal responses. American Naturalist 178, 668–678.CrossRefGoogle ScholarPubMed
Forster, J., Hirst, A. G. and Atkinson, D. (2012). Warming-induced reductions in body size are greater in aquatic than terrestrial species. Proceedings of the National Academy of Sciences of the United States of America 109, 19310–19314.Google Scholar
Fredensborg, B. L. and Poulin, R. (2005). Larval helminths in intermediate hosts: does competition early in life determine the fitness of adult parasites? International Journal for Parasitology 35, 1061–1070.Google Scholar
Freeman, R. S. (1952). Temperature as a factor affecting development of Monoecocestus (Cestoda: Anoplocephalidae) in oribatid mites. Experimental Parasitology 1, 256–262.Google Scholar
Frenkel, J. K. and Dubey, J. P. (2000). The taxonomic importance of obligate heteroxeny: distinction of Hammondia hammondi from Toxoplasma gondii – another opinion. Parasitology Research 86, 783–786.Google Scholar
Froyd, G. and Round, M. C. (1960). The artificial infection of adult cattle with Cysticercus bovis . Research in Veterinary Science 1, 275–282.Google Scholar
Gandon, S. (2004). Evolution of multihost parasites. Evolution 58, 455–469.Google Scholar
Geffen, A. J., van der Veer, H. W. and Nash, R. D. M. (2007). The cost of metamorphosis in flatfishes. Journal of Sea Research 58, 35–45.Google Scholar
Ghazal, A. M. and Avery, R. A. (1974). Population dynamics of Hymenolepis nana in mice: fecundity and the “crowding effect”. Parasitology 69, 403–415.Google Scholar
Ghosh, S. M., Testa, N. D. and Shingleton, A. W. (2013). Temperature-size rule is mediated by thermal plasticity of critical size in Drosophila melanogaster . Proceedings of the Royal Society B: Biological Sciences 280, 20130174.Google Scholar
Gibbs, H. C. (1986). Hypobiosis in parasitic nematodes—an update. Advances in Parasitology 25, 129–174.Google Scholar
Gilad, Y., Rifkin, S. A. and Pritchard, J. K. (2008). Revealing the architecture of gene regulation: the promise of eQTL studies. Trends in Genetics 24, 408–415.Google Scholar
Gismondi, E., Beisel, J. N. and Cossu-Leguille, C. (2012). Polymorphus minutus affects antitoxic responses of Gammarus roeseli exposed to Cadmium. PLoS ONE 7, e41475.Google Scholar
Goater, C. P. (1994). Growth and survival of postmetamorphic toads: interactions among larval history, density, and parasitism. Ecology 75, 2264–2274.Google Scholar
Goldberg, E. E., Kohn, J. R., Lande, R., Robertson, K. A., Smith, S. A. and Igić, B. (2010). Species selection maintains self-incompatibility. Science 330, 493–495.Google Scholar
Gomez-Mestre, I., Saccoccio, V. L., Iljima, T., Collins, E. M., Rosenthal, G. G. and Warkentin, K. M. (2010). The shape of things to come: linking developmental plasticity to post-metamorphic morphology in anurans. Journal of Evolutionary Biology 23, 1364–1373.Google Scholar
Gorton, M. J., Kasl, E. L., Detwiler, J. T. and Criscione, C. D. (2012). Testing local-scale panmixia provides insights into the cryptic ecology, evolution, and epidemiology of metazoan animal parasites. Parasitology 139, 981–997.Google Scholar
Gould, S. J. (1977). Ontogeny and Phylogeny. Harvard University Press, Cambridge, Massachusetts.Google Scholar
Govindarajan, A. F., Boero, F. and Halanych, K. M. (2006). Phylogenetic analysis with multiple markers indicates repeated loss of the adult medusa stage in Campanulariidae (Hydrozoa, Cnidaria). Molecular Phylogenetics and Evolution 38, 820–834.Google Scholar
Gower, C. M. and Webster, J. P. (2004). Fitness of indirectly transmitted pathogens: restraint and constraint. Evolution 58, 1178–1184.Google Scholar
Graff, D. J. and Kitzman, W. B. (1965). Factors influencing the activation of acanthocephalan cystacanths. Journal of Parasitology 51, 424–429.Google Scholar
Grech, K., Watt, K. and Read, A. F. (2006). Host–parasite interactions for virulence and resistance in a malaria model system. Journal of Evolutionary Biology 19, 1620–1630.Google Scholar
Haeckel, E. (1868). Natürliche Schöpfungsgeschichte, 1st Edn. Georg Reimer, Berlin.Google Scholar
Hafer, N. and Benesh, D. P. (2015). Does resource availability affect host manipulation? – an experimental test with Schistocephalus solidus . Parasitology Open 1, e3.Google Scholar
Hall, N., Karras, M., Raine, J. D., Carlton, J. M., Kooij, T. W., Berriman, M., Florens, L., Janssen, C. S., Pain, A., Christophides, G. K., James, K., Rutherford, K., Harris, B., Harris, D., Churcher, C., Quail, M. A., Ormond, D., Doggett, J., Trueman, H. E., Mendoza, J., Bidwell, S. L., Rajandream, M. A., Carucci, D. J., Yates, J. R. III, Kafatos, F. C., Janse, C. J., Barrell, B., Turner, C. M., Waters, A. P. and Sinden, R. E. (2005). A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 307, 82–86.Google Scholar
Hammerschmidt, K. and Kurtz, J. (2005 a). Evolutionary implications of the adaptation to different immune systems in a parasite with a complex life cycle. Proceedings of the Royal Society B: Biological Sciences 272, 2511–2518.Google Scholar
Hammerschmidt, K. and Kurtz, J. (2005 b). Surface carbohydrate composition of a tapeworm in its consecutive intermediate hosts: individual variation and fitness consequences. International Journal for Parasitology 35, 1499–1507.Google Scholar
Hammerschmidt, K., Koch, K., Milinski, M., Chubb, J. C. and Parker, G. A. (2009). When to go: optimization of host switching in parasites with complex life cycles. Evolution 63, 1976–1986.Google Scholar
Hanelt, B. and Janovy, J. Jr. (2004). Untying a Gordian knot: the domestication and laboratory maintenance of a gordian worm, Paragordius varius (Nematomorpha: Gordiida). Journal of Natural History 38, 939–950.Google Scholar
Hanzelová, V. and Zitnan, R. (1986). Embryogenesis and development of Bothriocephalus acheilognathi Yamaguti, 1934 (Cestoda) in the intermediate host under experimental conditions. Helminthologia 23, 145–155.Google Scholar
Hardy, N. B., Peterson, D. A. and von Dohlen, C. D. (2015). The evolution of life cycle complexity in aphids: ecological optimization or historical constraint? Evolution 69, 1423–1432.Google Scholar
Harvey, S. C., Gemmill, A. W., Read, A. F. and Viney, M. E. (2000). The control of morph development in the parasitic nematode Strongyloides ratti . Proceedings of the Royal Society B: Biological Sciences 267, 2057–2063.Google Scholar
Heins, D., Baker, J. and Martin, H. (2002). The “crowding effect” in the cestode Schistocephalus solidus: density-dependent effects on plerocercoid size and infectivity. Journal of Parasitology 88, 302–307.Google Scholar
Hendler, G. and Dojiri, M. (2009). The contrariwise life of a parasitic, pedomorphic copepod with a non-feeding adult: ontogenesis, ecology, and evolution. Invertebrate Biology 128, 65–82.CrossRefGoogle Scholar
Herrmann, K. K. and Poulin, R. (2011 a). Encystment site affects the reproductive strategy of a progenetic trematode in its fish intermediate host: is host spawning an exit for parasite eggs? Parasitology 138, 1183–1192.Google Scholar
Herrmann, K. K. and Poulin, R. (2011 b). Life cycle truncation in a trematode: does higher temperature indicate shorter host longevity? International Journal for Parasitology 41, 697–704.Google Scholar
Herrmann, K. K. and Poulin, R. (2012). The missing host hypothesis: do chemical cues from predators induce life cycle truncation of trematodes within their fish host? Journal of Fish Biology 80, 816–830.Google Scholar
Herrmann, K. K., Poulin, R., Keeney, D. B. and Blasco-Costa, I. (2014). Genetic structure in a progenetic trematode: signs of cryptic species with contrasting reproductive strategies. International Journal for Parasitology 44, 811–818.Google Scholar
Heyneman, D. and Voge, M. (1957). Glycogen distribution in cysticercoids of three hymenolepidid cestodes. Journal of Parasitology 43, 527–531.Google Scholar
Hilbish, T. J., Winn, E. P. and Rawson, P. (1993). Genetic variation and covariation during larval and juvenile growth in Mercenaria mercenaria . Marine Biology 115, 97–104.Google Scholar
Hopkins, C. A. (1952). Studies on cestode metabolism. II. The utilization of glycogen by Schistocephalus solidus in vitro . Experimental Parasitology 1, 196–213.CrossRefGoogle Scholar
Houle, D. (1991). Genetic covariance of fitness correlates: what genetic correlations are made of and why it matters. Evolution 45, 630–648.Google Scholar
Hunkeler, P. (1974). Les cestodes parasites des petits mammifères (Rongeurs et Insectivores) de Côte-d'Ivoire et de Haute-Volta. Revue Suisse de Zoologie. 80, 809–930.Google Scholar
Hunninen, A. V. (1935). Studies on the life history and host–parasite relations of Hymenolepis fraterna (H. nana, var. fraterna, Stiles) in white mice. American Journal of Hygiene 22, 414–443.Google Scholar
Iglesias, L., Valero, A., Benítez, R. and Adroher, F. J. (2001). In vitro cultivation of Anisakis simplex: pepsin increases survival and moulting from fourth larval to adult stage. Parasitology 123, 285–291.Google Scholar
Istock, C. A. (1967). The evolution of complex life cycle phenomena: an ecological perspective. Evolution 21, 592–605.Google Scholar
Iwasa, Y. and Wada, G. (2006). Complex life cycle and body sizes at life-history transitions for macroparasites. Evolutionary Ecology Research 8, 1427–1443.Google Scholar
Jablonski, D. and Hunt, G. (2006). Larval ecology, geographic range, and species survivorship in Cretaceous mollusks: organismic versus species-level explanations. American Naturalist 168, 556–564.Google Scholar
Jackson, A. P. (2010). The evolution of amastin surface glycoproteins in trypanosomatid parasites. Molecular Biology and Evolution 27, 33–45.Google Scholar
Jakobsen, P. J., Scharsack, J. P., Hammerschmidt, K., Deines, P., Kalbe, M. and Milinski, M. (2012). In vitro transition of Schistocephalus solidus (Cestoda) from coracidium to procercoid and from procercoid to plerocercoid. Experimental Parasitology 130, 267–273.Google Scholar
Janwan, P., Intapan, P. M., Sanpool, O., Sadaow, L., Thanchomnang, T. and Maleewong, W. (2011). Growth and development of Gnathostoma spinigerum (Nematoda: Gnathostomatidae) larvae in Mesocyclops aspericornis (Cyclopoida: Cyclopidae). Parasites & Vectors 4, 93.Google Scholar
Jeffery, C. H. and Emlet, R. B. (2003). Macroevolutionary consequences of developmental mode in temnopleurid echinoids from the tertiary of southern Australia. Evolution 57, 1031–1048.Google Scholar
Jennings, J. and Calow, P. (1975). The relationship between high fecundity and the evolution of entoparasitism. Oecologia 115, 109–115.Google Scholar
Johnson, P. T. J., Chase, J. M., Dosch, K. L., Hartson, R. B., Gross, J. A., Larson, D. J., Sutherland, D. R. and Carpenter, S. R. (2007). Aquatic eutrophication promotes pathogenic infection in amphibians. Proceedings of the National Academy of Sciences of the United States of America 104, 15781–15786.Google Scholar
Johnson, D. W., Christie, M. R., Moye, J. and Hixon, M. A. (2011). Genetic correlations between adults and larvae in a marine fish: potential effects of fishery selection on population replenishment. Evolutionary Applications 4, 621–633.CrossRefGoogle Scholar
Jolly, E. R., Chin, C.-S., Miller, S., Bahgat, M. M., Lim, K. C., DeRisi, J. and McKerrow, J. H. (2007). Gene expression patterns during adaptation of a helminth parasite to different environmental niches. Genome Biology 8, R65.Google Scholar
Joyeux, C. and Baer, J. G. (1936). Faune de France: Cestodes. Paul Lechevalier et Fils, Paris, France.Google Scholar
Kadota, K., Ishino, T., Matsuyama, T., Chinzei, Y. and Yuda, M. (2004). Essential role of membrane-attack protein in malarial transmission to mosquito host. Proceedings of the National Academy of Sciences of the United States of America 101, 16310–16315.Google Scholar
Kariu, T., Ishino, T., Yano, K., Chinzei, Y. and Yuda, M. (2006). CelTOS, a novel malarial protein that mediates transmission to mosquito and vertebrate hosts. Molecular Microbiology 59, 1369–1379.Google Scholar
Kasl, E. L., McAllister, C. T., Robison, H. W., Connior, M. B., Font, W. F. and Criscione, C. D. (2015). Evolutionary consequence of a change in life cycle complexity: a link between precocious development and evolution toward female-biased sex allocation in a hermaphroditic parasite. Evolution 69, 3156–3170.Google Scholar
Kazacos, K. (2001). Baylisascaris procyonis and related species. In Parasitic Diseases of Wild Mammals (ed. Samuel, W., Pybus, M. and Kocan, A.), pp. 301–341. Iowa State University Press, Ames, Iowa.Google Scholar
Keas, B. E. and Esch, G. W. (1997). The effect of diet and reproductive maturity on the growth and reproduction of Helisoma anceps (Pulmonata) infected by Halipegus occidualis (Trematoda). Journal of Parasitology 83, 96–104.CrossRefGoogle ScholarPubMed
Keeney, D. B., Waters, J. M. and Poulin, R. (2007). Clonal diversity of the marine trematode Maritrema novaezealandensis within intermediate hosts: the molecular ecology of parasite life cycles. Molecular Ecology 16, 431–439.Google Scholar
Kennedy, C. (1965). The life history of Archigetes limnodrili (Yamaguti)(Cestoda: Caryophyllaeidae) and its development in the invertebrate host. Parasitology 55, 427–437.Google Scholar
Keymer, A. (1981). Population dynamics of Hymenolepis diminuta in the intermediate host. Journal of Animal Ecology 50, 941–950.Google Scholar
Koehler, A. V., Brown, B., Poulin, R., Thieltges, D. W. and Fredensborg, B. L. (2012). Disentangling phylogenetic constraints from selective forces in the evolution of trematode transmission stages. Evolutionary Ecology 26, 1497–1512.Google Scholar
Køie, M. (1993). Aspects of the life cycle and morphology of Hysterothylacium aduncum (Rudolphi, 1802) (Nematoda, Ascaridoidea, Anisakidae). Canadian Journal of Zoology 71, 1289–1296.Google Scholar
Køie, M. and Fagerholm, H. P. (1995). The life cycle of Contracaecum osculatum (Rudolphi, 1802) sensu stricto (Nematoda, Ascaridoidea, Anisakidae) in view of experimental infections. Parasitology Research 81, 481–489.Google Scholar
Kollien, A. H. and Schaub, G. (1998). The development of Trypanosoma cruzi (Trypanosomatidae) in the reduviid bug Triatoma infestans (Insecta): influence of starvation. Journal of Eukaryotic Microbiology 45, 59–63.Google Scholar
Koudela, B. and Modrý, D. (2000). Sarcocystis muris possesses both diheteroxenous and dihomoxenous characters of life cycle. Journal of Parasitology 86, 877–879.Google Scholar
Kriska, T. (1993). Parasitic helminths of house mouse (Mus musculus Linnaeus, 1758) in Hungary. Miscellanea Zoologica Hungarica 8, 13–23.Google Scholar
Kurtz, J., Kalbe, M., Aeschlimann, P. B., Häberli, M. A., Wegner, K. M., Reusch, T. B. H., and Milinski, M. (2004). Major histocompatibility complex diversity influences parasite resistance and innate immunity in sticklebacks. Proceedings of the Royal Society B: Biological Sciences 271, 197–204.Google Scholar
Labaude, S., Cézilly, F., Tercier, X. and Rigaud, T. (2015). Influence of host nutritional condition on post-infection traits in the association between the manipulative acanthocephalan Pomphorhynchus laevis and the amphipod Gammarus pulex . Parasites & Vectors 8, 403.Google Scholar
Lackie, J. M. (1972). The course of infection and growth of Moniliformis dubius (Acanthocephala) in the intermediate host Periplaneta americana . Parasitology 64, 95–106.Google Scholar
Lagrue, C. and Poulin, R. (2007). Life cycle abbreviation in the trematode Coitocaecum parvum: can parasites adjust to variable conditions? Journal of Evolutionary Biology 20, 1189–1195.Google Scholar
Lagrue, C. and Poulin, R. (2008). Intra-and interspecific competition among helminth parasites: effects on Coitocaecum parvum life history strategy, size and fecundity. International Journal for Parasitology 38, 1435–1444.Google Scholar
Lagrue, C. and Poulin, R. (2009 a). Life cycle abbreviation in trematode parasites and the developmental time hypothesis: is the clock ticking? Journal of Evolutionary Biology 22, 1727–1738.Google Scholar
Lagrue, C. and Poulin, R. (2009 b). Heritability and short-term effects of inbreeding in the progenetic trematode Coitocaecum parvum: is there a need for the definitive host? Parasitology 136, 231–240.Google Scholar
Lagrue, C., Poulin, R. and Keeney, D. B. (2009). Effects of clonality in multiple infections on the life-history strategy of the trematode Coitocaecum parvum in its amphipod intermediate host. Evolution 63, 1417–1426.Google Scholar
Lambert, K. A., Pathak, A. K. and Cattadori, I. M. (2015). Does host immunity influence helminth egg hatchability in the environment? Journal of Helminthology 89, 446–452.Google Scholar
Lambrechts, L., Fellous, S. and Koella, J. C. (2006). Coevolutionary interactions between host and parasite genotypes. Trends in Parasitology 22, 12–16.Google Scholar
Lande, R. (1979). Quantitative genetic analysis of multivariate evolution, applied to brain: body size allometry. Evolution 33, 402–416.Google Scholar
Leclere, L., Schuchert, P., Cruaud, C., Couloux, A. and Manuel, M. (2009). Molecular phylogenetics of Thecata (Hydrozoa, Cnidaria) reveals long-term maintenance of life history traits despite high frequency of recent character changes. Systematic Biology 58, 509–526.Google Scholar
Lefebvre, F. and Poulin, R. (2005). Progenesis in digenean trematodes: a taxonomic and synthetic overview of species reproducing in their second intermediate hosts. Parasitology 130, 587–605.Google Scholar
Lei, F. and Poulin, R. (2011). Effects of salinity on multiplication and transmission of an intertidal trematode parasite. Marine Biology 158, 995–1003.Google Scholar
Levsen, A. and Jakobsen, P. J. (2002). Selection pressure towards monoxeny in Camallanus cotti (Nematoda, Camallanidae) facing an intermediate host bottleneck situation. Parasitology 124, 625–629.Google Scholar
Li, W. H., Yang, J. and Gu, X. (2005). Expression divergence between duplicate genes. Trends in Genetics 21, 602–607.CrossRefGoogle ScholarPubMed
Little, T., Birch, J., Vale, P. and Tseng, M. (2007). Parasite transgenerational effects on infection. Evolutionary Ecology Research 9, 459–469.Google Scholar
Lively, C. M. and Dybdahl, M. F. (2000). Parasite adaptation to locally common host genotypes. Nature 405, 679–681.Google Scholar
Loker, E. S. (1983). A comparative study of the life-histories of mammalian schistosomes. Parasitology 87, 343–369.Google Scholar
Louhi, K. R., Karvonen, A., Rellstab, C. and Jokela, J. (2013). Genotypic and phenotypic variation in transmission traits of a complex life cycle parasite. Ecology and Evolution 3, 2116–2127.Google Scholar
Luijckx, P., Ben-Ami, F., Mouton, L., Du Pasquier, L. and Ebert, D. (2011). Cloning of the unculturable parasite Pasteuria ramosa and its Daphnia host reveals extreme genotype-genotype interactions. Ecology Letters 14, 125–131.Google Scholar
Lynch, M. and Walsh, B. (1998). Genetics and Analysis of Quantitative Traits. Sinauer Associates, Inc., Sunderland.Google Scholar
Mackay, T. F. C., Stone, E. A. and Ayroles, J. F. (2009). The genetics of quantitative traits: challenges and prospects. Nature Reviews Genetics 10, 565–577.Google Scholar
Mackiewicz, J. S. (1988). Cestode transmission patterns. Journal of Parasitology 74, 60–71.Google Scholar
Mackinnon, M. J. and Read, A. F. (2004). Immunity promotes virulence evolution in a malaria model. PLoS Biology 2, e230.Google Scholar
Marden, J. H. (2000). Variability in the size, composition, and function of insect flight muscles. Annual Review of Physiology 62, 157–178.Google Scholar
Marshall, D. (2008). Transgenerational plasticity in the sea: context-dependent maternal effects across the life history. Ecology 89, 418–427.Google Scholar
Marshall, D. J. and Keough, M. J. (2004). Variable effects of larval size on post-metamorphic performance in the field. Marine Ecology Progress Series 279, 73–80.Google Scholar
Marshall, D. J. and Morgan, S. G. (2011). Ecological and evolutionary consequences of linked life-history stages in the sea. Current Biology 21, R718–R725.Google Scholar
Marshall, D. J., Krug, P. J., Kupriyanova, E., Byrne, M. and Emlet, R. B. (2012). The biogeography of marine invertebrate life histories. Annual Review of Ecology, Evolution, and Systematics 43, 97–114.Google Scholar
Matuschka, F. R. and Bannert, B. (1987). Cannibalism and autotomy as predator–prey relationship for monoxenous sarcosporidia. Parasitology Research 74, 88–93.Google Scholar
McEdward, L. R. and Miner, B. G. (2001). Larval and life-cycle patterns in echinoderms. Canadian Journal of Zoology 79, 1125–1170.Google Scholar
McLaughlin, J. D., Marcogliese, D. J. and Kelly, J. (2006). Morphological, developmental and ecological evidence for a progenetic life cycle in Neochasmus (Digenea). Folia Parasitologica 53, 44–52.Google Scholar
McMillan, W. O., Raff, R. A. and Palumbi, S. R. (1992). Population genetic consequences of developmental evolution in sea urchins (genus Heliocidaris). Evolution 46, 1299–1312.Google Scholar
Mead, R. W. and Olsen, O. W. (1971). The life cycle and development of Ophiotaenia filaroides (La Rue, 1919) (Protocephala: Proteocephalidae). Journal of Parasitology 57, 869–874.Google Scholar
Merkey, A. B., Wong, C. K., Hoshizaki, D. K. and Gibbs, A. G. (2011). Energetics of metamorphosis in Drosophila melanogaster . Journal of Insect Physiology 57, 1437–1445.Google Scholar
Michaud, M., Milinski, M., Parker, G. A. and Chubb, J. C. (2006). Competitive growth strategies in intermediate hosts: experimental tests of a parasite life-history model using the cestode, Schistocephalus solidus . Evolutionary Ecology 20, 39–57.Google Scholar
Michel, J. F. (1974). Arrested development of nematodes and some related phenomena. Advances in Parasitology 12, 279–366.Google Scholar
Minning, T. A., Weatherly, D. B., Atwood, J., Orlando, R. and Tarleton, R. L. (2009). The steady-state transcriptome of the four major life-cycle stages of Trypanosoma cruzi . BMC Genomics 10, 370.Google Scholar
Molnár, P. K., Dobson, A. P. and Kutz, S. J. (2013). Gimme shelter – the relative sensitivity of parasitic nematodes with direct and indirect life cycles to climate change. Global Change Biology 19, 3291–3305.Google Scholar
Moore, J. (1981). Asexual reproduction and environmental predictability in cestodes (Cyclophyllidea, Taeniidae). Evolution 35, 723–741.Google Scholar
Moorthy, V. N. (1938). Observations on the life history of Camallanus sweeti . Journal of Parasitology 24, 323–342.Google Scholar
Moran, N. A. (1991). Phenotype fixation and genotypic diversity in the complex life cycle of the aphid Pemphigus betae . Evolution 45, 957–970.Google Scholar
Moran, N. A. (1994). Adaptation and constraint in the complex life cycles of animals. Annual Review of Ecology and Systematics 25, 573–600.Google Scholar
Morand, S., Robert, F. and Connors, V. A. (1995). Complexity in parasite life cycles: population biology of cestodes in fish. Journal of Animal Ecology 64, 256–264.Google Scholar
Morand, S., Legendre, P., Gardner, S. L. and Hugot, J. P. (1996). Body size evolution of oxyurid (Nematoda) parasites: the role of hosts. Oecologia 107, 274–282.Google Scholar
Moravec, F., Prokopic, J. and Shlikas, A. V. (1987). The biology of nematodes of the family Capillariidae Neveu-Lemaire, 1936. Folia Parasitologica 34, 39–56.Google Scholar
Mordecai, E. A., Paaijmans, K. P., Johnson, L. R., Balzer, C., Ben-Horin, T., de Moor, E., Mcnally, A., Pawar, S., Ryan, S. J., Smith, T. C. and Lafferty, K. D. (2013). Optimal temperature for malaria transmission is dramatically lower than previously predicted. Ecology Letters 16, 22–30.Google Scholar
Morley, N. J. and Lewis, J. W. (2015). Thermodynamics of trematode infectivity. Parasitology 142, 585–597.Google Scholar
Mousseau, T. and Fox, C. (1998). Maternal Effects as Adaptations. (ed. Mousseau, T. and Fox, C.) Oxford University Press, Oxford.Google Scholar
Mueller, J. F. (1966). Laboratory propagation of Spirometra mansonoides (Mueller 1935) as an experimental tool. VII. Improved techniques and additional notes on the biology of the cestode. Journal of Parasitology 52, 437–443.Google Scholar
Mulcahy, G., O'Neill, S., Fanning, J., McCarthy, E. and Sekiya, M. (2005). Tissue migration by parasitic helminths – an immunoevasive strategy? Trends in Parasitology 21, 273–277.Google Scholar
O'Connor, C. M., Norris, D. R., Crossin, G. T. and Cooke, S. J. (2014). Biological carryover effects: linking common concepts and mechanisms in ecology and evolution. Ecosphere 5, 28.Google Scholar
Palm, H. W. (2004). The Trypanorhyncha Diesing, 1863. PKSPL-IPB, Bogor.Google Scholar
Palm, H. W. and Caira, J. N. (2008). Host specificity of adult versus larval cestodes of the elasmobranch tapeworm order Trypanorhyncha. International Journal for Parasitology 38, 381–388.Google Scholar
Pampoulie, C., Lambert, A., Rosecchi, E., Crivelli, A. J., Bouchereau, J.-L. and Morand, S. (2000). Host death: a necessary condition for the transmission of Aphalloides coelomicola Dollfus, Chabaud, and Golvan, 1957 (Digenea, Cryptogonimidae)? Journal of Parasitology 86, 416–417.Google Scholar
Pandian, T. J. and Marian, M. P. (1985). Time and energy costs of metamorphosis in the Indian Bullfrog Rana tigrina . Copeia 3, 653–662.Google Scholar
Park, J.-K., Kim, K.-H., Kang, S., Kim, W., Eom, K. S. and Littlewood, D. T. J. (2007). A common origin of complex life cycles in parasitic flatworms: evidence from the complete mitochondrial genome of Microcotyle sebastis (Monogenea: Platyhelminthes). BMC Evolutionary Biology 7, 11.Google Scholar
Parker, G. A., Chubb, J. C., Roberts, G. N., Michaud, M. and Milinski, M. (2003 a). Optimal growth strategies of larval helminths in their intermediate hosts. Journal of Evolutionary Biology 16, 47–54.Google Scholar
Parker, G. A., Chubb, J. C., Ball, M. A. and Roberts, G. N. (2003 b). Evolution of complex life cycles in helminth parasites. Nature 425, 480–484.Google Scholar
Parker, G. A., Ball, M. A. and Chubb, J. C. (2009 a). To grow or not to grow? Intermediate and paratenic hosts as helminth life cycle strategies. Journal of Theoretical Biology 258, 135–147.Google Scholar
Parker, G. A., Ball, M. A. and Chubb, J. C. (2009 b). Why do larval helminths avoid the gut of intermediate hosts? Journal of Theoretical Biology 260, 460–473.Google Scholar
Parker, G. A., Ball, M. A. and Chubb, J. C. (2015 a). Evolution of complex life cycles in trophically transmitted helminths. I. Host incorporation and trophic ascent. Journal of Evolutionary Biology 28, 267–291.Google Scholar
Parker, G. A., Ball, M. A. and Chubb, J. C. (2015 b). Evolution of complex life cycles in trophically transmitted helminths. II. How do life-history stages adapt to their hosts? Journal of Evolutionary Biology 28, 292–304.Google Scholar
Paull, S. H., Lafonte, B. E. and Johnson, P. T. J. (2012). Temperature-driven shifts in a host-parasite interaction drive nonlinear changes in disease risk. Global Change Biology 18, 3558–3567.Google Scholar
Pechenik, J. A. (2006). Larval experience and latent effects – metamorphosis is not a new beginning. Integrative and Comparative Biology 46, 323–333.Google Scholar
Pechenik, J. A. and Fried, B. (1995). Effect of temperature on survival and infectivity of Echinostoma trivolvis cercariae: a test of the energy limitation hypothesis. Parasitology 111, 373–378.Google Scholar
Perkins, E. M., Donnellan, S. C., Bertozzi, T. and Whittington, I. D. (2010). Closing the mitochondrial circle on paraphyly of the Monogenea (Platyhelminthes) infers evolution in the diet of parasitic flatworms. International Journal for Parasitology 40, 1237–1245.Google Scholar
Perrot-Minnot, M.-J., Gaillard, M., Dodet, R. and Cézilly, F. (2011). Interspecific differences in carotenoid content and sensitivity to UVB radiation in three acanthocephalan parasites exploiting a common intermediate host. International Journal for Parasitology 41, 173–181.Google Scholar
Phillips, P. C. (1998). Genetic constraints at the metamorphic boundary: morphological development in the wood frog, Rana sylvatica . Journal of Evolutionary Biology 11, 453–463.Google Scholar
Phillips, N. E. (2002). Effects of nutrition-mediated larval condition on juvenile performance in a marine mussel. Ecology 83, 2562–2574.Google Scholar
Pietrock, M. and Marcogliese, D. J. (2003). Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology 19, 293–299.Google Scholar
Podolsky, R. D. and Moran, A. L. (2006). Integrating function across marine life cycles. Integrative and Comparative Biology 46, 577–586.Google Scholar
Pollitt, L. C., MacGregor, P., Matthews, K. and Reece, S. E. (2011). Malaria and trypanosome transmission: different parasites, same rules? Trends in Parasitology 27, 197–203.Google Scholar
Poulin, R. (1992). Determinants of host-specificity in parasites of freshwater fishes. International Journal for Parasitology 22, 753–758.Google Scholar
Poulin, R. (2003). Information about transmission opportunities triggers a life-history switch in a parasite. Evolution 57, 2899–2903.Google Scholar
Poulin, R. and Cribb, T. H. (2002). Trematode life cycles: short is sweet? Trends in Parasitology 18, 176–183.Google Scholar
Poulin, R. and Latham, A. D. M. (2003). Effects of initial (larval) size and host body temperature on growth in trematodes. Canadian Journal of Zoology 81, 574–581.Google Scholar
Poulin, R. and Lefebvre, F. (2006). Alternative life-history and transmission strategies in a parasite: first come, first served? Parasitology 132, 135–141.Google Scholar
Poulin, R., Wise, M. and Moore, J. (2003 a). A comparative analysis of adult body size and its correlates in acanthocephalan parasites. International Journal for Parasitology 33, 799–805.Google Scholar
Poulin, R., Nichol, K. and Latham, A. D. A. (2003 b). Host sharing and host manipulation by larval helminths in shore crabs: cooperation or conflict? International Journal for Parasitology 33, 425–433.Google Scholar
Pugh, R. E. (1987). Effects on the development of Dipylidium caninum and on the host reaction to this parasite in the adult flea (Ctenocephalides felis felis). Parasitology Research 73, 171–177.Google Scholar
Quinn, T. P., Kendall, N. W., Rich, H. B. and Chasco, B. E. (2012). Diel vertical movements, and effects of infection by the cestode Schistocephalus solidus on daytime proximity of three-spined sticklebacks Gasterosteus aculeatus to the surface of a large Alaskan lake. Oecologia 168, 43–51.Google Scholar
Raff, R. A. and Byrne, M. (2006). The active evolutionary lives of echinoderm larvae. Heredity 97, 244–252.Google Scholar
Randhawa, H. S. and Poulin, R. (2009). Determinants and consequences of interspecific body size variation in tetraphyllidean tapeworms. Oecologia 161, 759–769.Google Scholar
Rauch, G., Kalbe, M. and Reusch, T. B. H. (2005). How a complex life cycle can improve a parasite's sex life. Journal of Evolutionary Biology 18, 1069–1075.Google Scholar
Read, A. F. and Skorping, A. (1995). The evolution of tissue migration by parasitic nematode larvae. Parasitology 111, 359–371.Google Scholar
Reim, C., Teuschl, Y. and Blanckenhorn, W. U. (2006). Size-dependent effects of temperature and food stress on energy reserves and starvation resistance in yellow dung flies. Evolutionary Ecology Research 8, 1215–1234.Google Scholar
Reiss, J. O. (2002). The phylogeny of amphibian metamorphosis. Zoology 105, 85–96.Google Scholar
Relyea, R. A. (2007). Getting out alive: how predators affect the decision to metamorphose. Oecologia 152, 389–400.Google Scholar
Revell, L. J., Harmon, L. J. and Collar, D. C. (2008). Phylogenetic signal, evolutionary process, and rate. Systematic Biology 57, 591–601.Google Scholar
Richter-Boix, A., Orizaola, G. and Laurila, A. (2014). Transgenerational phenotypic plasticity links breeding phenology with offspring life-history. Ecology 95, 2815–2825.Google Scholar
Rietschel, G. (1973). Untersuchungen zur Entwicklung einiger in Krähen (Corvidae) vorkommender Nematoden. Zeitschrift für Parasitenkunde 42, 243–250.Google Scholar
Roberts, L. S., Janovy, J. Jr. and Nadler, S. (2013). Foundations of Parasitology, 9th Edn. McGraw-Hill Higher Education, New York, NY.Google Scholar
Roff, D. (1997). Evolutionary Quantitative Genetics. Chapman and Hall, New York.Google Scholar
Roff, D. A. and Fairbairn, D. J. (2007). The evolution of trade-offs: where are we? Journal of Evolutionary Biology 20, 433–447.Google Scholar
Rolff, J., de Meutter, F. and Stoks, R. (2004). Time constraints decouple age and size at maturity and physiological traits. American Naturalist 164, 559–565.Google Scholar
Rosen, R. and Dick, T. A. (1983). Development and infectivity of the procercoid of Triaenophorus crassus Forel and mortality of the first intermediate host. Canadian Journal of Zoology 61, 2120–2128.Google Scholar
Rossiter, M. (1996). Incidence and consequences of inherited environmental effects. Annual Review of Ecology and Systematics 27, 451–476.Google Scholar
Rowe, L. and Ludwig, D. (1991). Size and timing of metamorphosis in complex life cycles: time constraints and variation. Ecology 72, 413–427.Google Scholar
Rudolf, V. H. W. and Rödel, M.-O. (2007). Phenotypic plasticity and optimal timing of metamorphosis under uncertain time constraints. Evolutionary Ecology 21, 121–142.Google Scholar
Sandeman, I. M. and Burt, M. D. B. (1972). Biology of Bothrimonus (=Diplocotyle) (Pseudophyllidea: Cestoda): ecology, life cycle, and evolution; a review and synthesis. Journal Fisheries Research Board of Canada 29, 1381–1395.Google Scholar
Sandland, G. J. and Minchella, D. J. (2003). Effects of diet and Echinostoma revolutum infection on energy allocation patterns in juvenile Lymnaea elodes snails. Oecologia 134, 479–486.Google Scholar
Schärer, L., Karlsson, L. M., Christen, M. and Wedekind, C. (2001). Size-dependent sex allocation in a simultaneous hermaphrodite parasite. Journal of Evolutionary Biology 14, 55–67.Google Scholar
Schjørring, S. (2004). Delayed selfing in relation to the availability of a mating partner in the cestode Schistocephalus solidus . Evolution 58, 2591–2596.Google Scholar
Schjørring, S. and Lüscher, A. (2003). Schistocephalus solidus: a molecular test of premature gamete exchange for fertilization in the intermediate host Gasterosteus aculeatus . Experimental Parasitology 103, 174–176.Google Scholar
Schmidt, G. (1985). Development and life cycles. In Biology of the Acanthocephala (ed. Crompton, D. W. T. and Nickol, B. B.), pp. 273–305. Cambridge University Press, Cambridge.Google Scholar
Scholz, T. (1997). Life-cycle of Bothriocephalus claviceps, a specific parasite of eels. Journal of Helminthology 71, 241–248.Google Scholar
Seppälä, O., Liljeroos, K., Karvonen, A. and Jokela, J. (2008). Host condition as a constraint for parasite reproduction. Oikos 117, 749–753.Google Scholar
Shostak, A. W. and Dick, T. A. (1986). Effect of food intake by Cyclops bicuspidatus thomasi (Copepoda) on growth of proceroids of Triaenophorus crassus (Pseudophyllidea) and on host fecundity. American Midland Naturalist 115, 225–233.Google Scholar
Shostak, A. W., Rosen, R. B. and Dick, T. A. (1985). The use of growth curves to assess the crowding effect on procercoids of the tapeworm Triaenophorus crassus in the copepod host Cyclops bicuspidatus thomasi . Canadian Journal of Zoology 63, 2343–2351.Google Scholar
Shostak, A. W., Walsh, J. G. and Wong, Y. C. (2008). Manipulation of host food availability and use of multiple exposures to assess the crowding effect on Hymenolepis diminuta in Tribolium confusum . Parasitology 135, 1019–1033.Google Scholar
Slapeta, J. R., Modry, D., Votypka, J., Jirku, M., Koudela, B. and Lukes, J. (2001). Multiple origin of the dihomoxenous life cycle in sarcosporidia. International Journal for Parasitology 31, 413–417.Google Scholar
Smith, J. W., Elarifi, A. E., Wootten, R., Pike, A. W. and Burt, M. D. B. (1990). Experimental infection of rainbow trout, Oncorhynchus mykiss, with Contracaecum osculatum (Rudolphi, 1802) and Pseudoterranova decipiens (Krabbe, 1878) (Nematoda: Ascaridoidea). Canadian Journal of Fisheries and Aquatic Sciences 47, 2293–2296.Google Scholar
Smyth, J. D. (1949). Studies on tapeworm physiology IV. Further observations on the development of Ligula intestinalis in vitro . Journal of Experimental Biology 26, 1–15.Google Scholar
Smyth, J. D. (1952). Studies on tapeworm physiology VI. Effect of temperature on the maturation in vitro of Schistocephalus solidus . Journal of Experimental Biology 29, 304–309.Google Scholar
Smythe, A. B. and Font, W. F. (2001). Phylogenetic analysis of Alloglossidium (Digenea: Macroderoididae) and related genera: life-cycle evolution and taxonomic revision. Journal of Parasitology 87, 386–391.Google Scholar
Spence, P. J., Jarra, W., Lévy, P., Reid, A. J., Chappell, L., Brugat, T., Sanders, M., Berriman, M. and Langhorne, J. (2013). Vector transmission regulates immune control of Plasmodium virulence. Nature 498, 228–231.Google Scholar
Sprehn, C. G., Blum, M. J., Quinn, T. P. and Heins, D. C. (2015). Landscape genetics of Schistocephalus solidus parasites in threespine stickleback (Gasterosteus aculeatus) from Alaska. PLoS ONE 10, e0122307 doi: 10.1371/journal.pone.0122307.Google Scholar
Sprent, J. F. A. (1956). The life history and development of Toxocara cati (Schrank 1788) in the domestic cat. Parasitology 46, 54–78.Google Scholar
Sprent, J. F. A. (1958). Observations on the development of Toxocara canis (Werner, 1782) in the dog. Parasitology 48, 184–209.Google Scholar
Stamper, C. E., Downie, J. R., Stevens, D. J. and Monaghan, P. (2009). The effects of perceived predation risk on pre- and post-metamorphic phenotypes in the common frog. Journal of Zoology 277, 205–213.Google Scholar
Stefka, J., Hypsa, V. and Scholz, T. (2009). Interplay of host specificity and biogeography in the population structure of a cosmopolitan endoparasite: microsatellite study of Ligula intestinalis (Cestoda). Molecular Ecology 18, 1187–1206.Google Scholar
Steinauer, M. L. and Nickol, B. B. (2003). Effect of cystacanth body size on adult success. Journal of Parasitology 89, 251–254.Google Scholar
Stigge, H. A. and Bolek, M. G. (2015). The alteration of life history traits and increased success of Halipegus eccentricus through the use of a paratenic host: a comparative study. Journal of Parasitology 101, 658–665.Google Scholar
Stoks, R. and Cordoba-Aguilar, A. (2012). Evolutionary ecology of Odonata: a complex life cycle perspective. Annual Review of Entomology 57, 249–265.Google Scholar
Studer, A. and Poulin, R. (2014). Analysis of trait mean and variability versus temperature in trematode cercariae: is there scope for adaptation to global warming? International Journal for Parasitology 44, 403–413.Google Scholar
Studer, A., Thieltges, D. W. and Poulin, R. (2010). Parasites and global warming: net effects of temperature on an intertidal host–parasite system. Marine Ecology Progress Series 415, 11–22.Google Scholar
Studer, A., Cubillos, V. M., Lamare, M. D., Poulin, R. and Burritt, D. J. (2012). Effects of ultraviolet radiation on an intertidal trematode parasite: an assessment of damage and protection. International Journal for Parasitology 42, 453–461.Google Scholar
Su, C., Evans, D., Cole, R. H., Kissinger, J. C., Ajioka, J. W. and Sibley, L. D. (2003). Recent expansion of Toxoplasma through enhanced oral transmission. Science 299, 414–416.Google Scholar
Sukhdeo, S., Sukhdeo, M., Black, M. and Vrijenhoek, R. (1997). The evolution of tissue migration in parasitic nematodes (Nematoda: Strongylida) inferred from a protein-coding mitochondrial gene. Biological Journal of the Linnean Society 61, 281–298.Google Scholar
Sures, B. and Radszuweit, H. (2007). Pollution-induced heat shock protein expression in the amphipod Gammarus roeseli is affected by larvae of Polymorphus minutus (Acanthocephala). Journal of Helminthology 81, 191–197.Google Scholar
Tenora, F. and Murai, E. (1970). Hymenolepis straminea (Goeze, 1782) (Cestoda, Hymenolepididae), parasite of Cricetus cricetus L. in Hungary. Parasitologia Hungarica 3, 33–42.Google Scholar
Thieltges, D. W. and Rick, J. (2006). Effect of temperature on emergence, survival and infectivity of cercariae of the marine trematode Renicola roscovita (Digenea: Renicolidae). Diseases of Aquatic Organisms 73, 63–68.Google Scholar
Thorson, G. (1950). Reproductive and larval ecology of marine bottom invertebrates. Biological Reviews 25, 1–45.Google Scholar
Tierney, J. and Crompton, D. (1992). Infectivity of plerocercoids of Schistocephalus solidus (Cestoda: Ligulidae) and fecundity of the adults in an experimental definitive host, Gallus gallus . Journal of Parasitology 78, 1049–1054.Google Scholar
Tigreros, N. (2013). Linking nutrition and sexual selection across life stages in a model butterfly system. Functional Ecology 27, 145–154.Google Scholar
Tinkle, D. (1972). Description and natural intermediate hosts of Hymenolepis peromysci n. sp., a new cestode from deer mice (Peromyscus). Transactions of the American Microscopical Society 91, 66–69.Google Scholar
Trouvé, S., Jourdane, J., Renaud, F., Durand, P. and Morand, S. (1999). Adaptive sex allocation in a simultaneous hermaphrodite. Evolution 53, 1599–1604.Google Scholar
Trouvé, S., Morand, S. and Gabrion, C. (2003). Asexual multiplication of larval parasitic worms: a predictor of adult life-history traits in Taeniidae? Parasitology Research 89, 81–88.Google Scholar
Tsai, I. J., Zarowiecki, M., Holroyd, N., Garciarrubio, A., Sanchez-Flores, A., Brooks, K. L., Tracey, A., Bobes, R. J., Fragoso, G., Sciutto, E., Aslett, M., Beasley, H., Bennett, H. M., Cai, J., Camicia, F., Clark, R., Cucher, M., De Silva, N., Day, T. A., Deplazes, P., Estrada, K., Fernández, C., Holland, P. W. H., Hou, J., Hu, S., Huckvale, T., Hung, S. S., Kamenetzky, L., Keane, J. A., Kiss, F. et al. (2013). The genomes of four tapeworm species reveal adaptations to parasitism. Nature 496, 57–63.Google Scholar
Tseng, M. (2006). Interactions between the parasite's previous and current environment mediate the outcome of parasite infection. American Naturalist 168, 565–571.Google Scholar
Twombly, S., Clancy, N. and Burns, C. W. (1998). Life history consequences of food quality in the freshwater copepod Boeckella triarticulata . Ecology 79, 1711–1724.Google Scholar
Valkounova, J. (1980). The most important factors affecting the larval development of cestodes of the family Hymenolepididae in crustaceans (Copepoda). Vĕst. čs. Společ. Zool. 44, 230–240.Google Scholar
Van Allen, B. G., Briggs, V. S., McCoy, M. W. and Vonesh, J. R. (2010). Carry-over effects of the larval environment on post-metamorphic performance in two hylid frogs. Oecologia 164, 891–898.Google Scholar
van der Have, T. M. and de Jong, G. (1996). Adult size in ectotherms: temperature effects on growth and differentiation. Journal of Theoretical Biology 183, 329–340.Google Scholar
Verástegui, M., González, A., Gilman, R. H., Gavidia, C., Falcón, N., Bernal, T. and Garcia, H. H. (2000). Experimental infection model for Taenia solium cysticercosis in swine. Veterinary Parasitology 94, 33–44.Google Scholar
Vickerman, K. (1965). Polymorphism and mitochondrial activity in sleeping sickness trypanosomes. Nature 208, 762–766.Google Scholar
Voge, M. and Heyneman, D. (1958). Effect of high temperature on the larval development of Hymenolepis nana and Hymenolepis diminuta (Cestoda: Cyclophyllidea). Journal of Parasitology 44, 249–260.Google Scholar
Wake, D. B. and Hanken, J. (1996). Direct development in the lungless salamanders: what are the consequences for developmental biology, evolution and phylogenesis? International Journal of Developmental Biology 40, 859–869.Google Scholar
Walker, S. M., Hoey, E., Fletcher, H., Brennan, G., Fairweather, I. and Trudgett, A. (2006). Stage-specific differences in fecundity over the life-cycle of two characterized isolates of the liver fluke, Fasciola hepatica . Parasitology 133, 209–216.Google Scholar
Walter, D. E. and Proctor, H. C. (2013). Mites: Ecology, Evolution & Behaviour. 2nd Edn. Springer, Dordrecht, doi: 10.1007/978-94-007-7164-2.Google Scholar
Walters, R. J. and Hassall, M. (2006). The temperature-size rule in ectotherms: may a general explanation exist after all? American Naturalist 167, 510–523.Google Scholar
Wang, C. L., Renaud, F., Thomas, F. (2002). Negative influence of Gammarinema gammari (Nematoda) on the fecundity of Microphallus papillorobustus (Trematoda): field and experimental evidence. Journal of Parasitology 88, 425–427.Google Scholar
Wassersug, R. J. and Sperry, D. G. (1977). The relationships of locomotion to differential predation on Pseudacris triseriata (Anura: Hylidae). Ecology 58, 830–839.Google Scholar
Watkins, T. B. (2001). A quantitative genetic test of adaptive decoupling across metamorphosis for locomotor and life-history traits in the Pacific tree frog, Hyla regilla . Evolution 55, 1668–1677.Google Scholar
Webster, J. P. and Woolhouse, M. E. J. (1998). Selection and strain specificity of compatibility between snail intermediate hosts and their parasitic schistosomes. Evolution 52, 1627–1634.Google Scholar
Wedekind, C., Christen, M., Schärer, L. and Treichel, N. (2000). Relative helminth size in crustacean hosts: in vivo determination, and effects of host gender and within-host competition in a copepod infected by a cestode. Aquatic Ecology 34, 279–285.Google Scholar
Weinersmith, K. L., Warinner, C. B., Tan, V., Harris, D. J., Mora, A. B., Kuris, A. M., Lafferty, K. D. and Hechinger, R. F. (2014). A lack of crowding? Body Size does not decrease with density for two behavior-manipulating parasites. Integrative and Comparative Biology 54, 184–192.Google Scholar
Werner, E. (1986). Amphibian metamorphosis: growth rate, predation risk, and the optimal size at transformation. American Naturalist 128, 319–341.Google Scholar
Werner, E. E. (1988). Size, scaling, and the evolution of complex life cycles. In Size-structured populations (ed. Ebenman, B. and Persson, L.), pp. 60–81. Springer, Berlin.Google Scholar
Werner, E. and Gilliam, J. (1984). The ontogenetic niche and species interactions in size-structured populations. Annual Review of Ecology and Systematics 15, 393–425.Google Scholar
Wheeler, W. C., Whiting, M. F., Wheeler, Q. D. and Carpenter, J. M. (2001). The phylogeny of the extant hexapod orders. Cladistics 17, 113–169.Google Scholar
Wiegmann, B. M., Trautwein, M. D., Kim, J.-W., Cassel, B. K., Bertone, M. A., Winterton, S. L. and Yeates, D. K. (2009). Single-copy nuclear genes resolve the phylogeny of the holometabolous insects. BMC Biology 7, 34.Google Scholar
Wiens, J., Bonett, R. and Chippindale, P. (2005). Ontogeny discombobulates phylogeny: paedomorphosis and higher-level salamander relationships. Systematic Biology 54, 91–110.Google Scholar
Wilbur, H. (1980). Complex life cycles. Annual review of Ecology and Systematics 11, 67–93.Google Scholar
Wolinska, J. and King, K. C. (2009). Environment can alter selection in host–parasite interactions. Trends in Parasitology 25, 236–244.Google Scholar
Wray, G. A. (1992). The evolution of larval morphology during the post-Paleozoic radiation of echinoids. Paleobiology 18, 258–287.Google Scholar
Wyatt, R. J. and Kennedy, C. R. (1988). The effects of a change in the growth rate of roach, Rutilus rutilus (L.), on the biology of the fish tapeworm Ligula intestinalis (L.). Journal of Fish Biology 33, 45–57.Google Scholar
Wygoda, J. A., Yang, Y., Byrne, M. and Wray, G. A. (2014). Transcriptomic analysis of the highly derived radial body plan of a sea urchin. Genome Biology and Evolution 6, 964–973.Google Scholar
Yang, A. S. (2001). Modularity, evolvability, and adaptive radiations: a comparison of the hemi- and holometabolous insects. Evolution & Development 3, 59–72.Google Scholar
Yoshinaga, T., Ogawa, K. and Wakabayashi, H. (1989). Life cycle of Hysterothylacium haze (Nematoda: Anisakidae: Raphidascaridinae). Journal of Parasitology 75, 756–763.Google Scholar
Zheng, H., Zhang, W., Zhang, L., Zhang, Z., Li, J., Lu, G., Zhu, Y., Wang, Y., Huang, Y., Liu, J., Kang, H., Chen, J., Wang, L., Chen, A., Yu, S., Gao, Z., Jin, L., Gu, W., Wang, Z., Zhao, L., Shi, B., Wen, H., Lin, R., Jones, M. K., Brejova, B., Vinar, T., Zhao, G., McManus, D. P., Chen, Z., Zhou, Y. et al. (2013). The genome of the hydatid tapeworm Echinococcus granulosus . Nature Genetics 45, 1168–1175.Google Scholar
Zuo, W., Moses, M. E., West, G. B., Hou, C. and Brown, J. H. (2012). A general model for effects of temperature on ectotherm ontogenetic growth and development. Proceedings of the Royal Society B: Biological Sciences 279, 1840–1846.Google Scholar