Abstract
Egg morphology varies among and within groups of parasites. Morphological variation is tightly coupled with transmission, and prior work suggests this variation is associated with host type and host habitat in some cases. Here, we used phylogenetic comparative methods combined with evolutionary model fitting to determine whether egg shape in acanthocephalans is constrained by evolutionary history and if this variation is a response to differences in habitat use among the intermediate host, definitive host, or a combination of the two. A model combining a phylogenetic reconstruction of 59 acanthocephalan species and life cycle data shows that egg shape is both constrained by evolutionary history and has evolved in response to the habitat (microhabitat) of the intermediate host. These results support the hypothesis that parasite egg morphology has adapted in response to host habitat and facilitates transmission.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11692-022-09595-9/MediaObjects/11692_2022_9595_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11692-022-09595-9/MediaObjects/11692_2022_9595_Fig2_HTML.png)
Similar content being viewed by others
Data Availability
All datasets and code to fully replicate this study are available at: https://github.com/alainapb/acanthocephalan_egg_shape_evo.
References
Amin, O. M. (1987). Key to the families and subfamilies of Acanthocephala, with the erection of a new class (Polyacanthocephala) and a new order (Polyacanthorhynchida). J Para, 73, 1216–1219.
Amin, O. M. (2013). Classification of the Acanthocephala. Folia Parasitologica, 60, 273–305.
Amin, O. M., Thielen, F., Münderle, M., Taraschewski, H., & Sures, B. (2008). Description of a new echinorhynchid species (Acanthocephala) from the european eel, Anguilla anguilla, in Germany, with a key to species of Acanthocephalus in Europe. J Para, 94, 1299–1304.
Arredondo, N. J., & Gil de Pertierra, A. A. (2009). Pseudoacanthocephalus lutzi (Hamann, 1891) comb. n. (Acanthocephala: Echinorhynchidae) of Acanthocephlaus lutzi (Hamann, 1891), parasite of South American amphibians. Folia Parasitologica, 56, 295–304.
Barger, M. A., & Nickol, B. B. (1998). Structure of Leptorhynchoides thecatus and Pomphorhynchus bulbocolli (Acanthocephala) eggs in habitat partitioning and transmission. J Para, 84(3), 534–537.
Barger, M. A., & Nickol, B. B. (1999). Effects of coinfection with Pomphorhynchus bulbocolli on development of Leptorhynchoides thecatus (Acanthocephala) in amphipods (Hyalella azteca). J Para, 85(1), 60–63.
Baylis, H. A. (1933). XLIII.—On some parasitic worms from Java, with remarks on the Acanthocephalan genus Pallisentis. Annals and Magazine of Natural History, 12(70), 443–449.
Bhalerao, G. D. (1931). LIX.—On a new species of Acanthocephala from Ophiocephalus striatus. Journal of Natural History, 7(42), 569–573.
Beaulieu, J. M., Jhwueng, D. C., Boettiger, C., & O’Meara, B. C. (2012). Modeling stabilizing selection: expanding the Ornstein–Uhlenbeck model of adaptive evolution. Evolution, 66(8), 2369–2383.
Blomberg, S. P., Garland, T. Jr., & Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution, 57(4), 717–745.
Bouckaert, R., Heled, J., Kühnert, D., Vaughan, T., Wu, C. H., **e, D., Suchard, M. A., Rambaut, A., & Drummond, A. J. (2014). BEAST 2: a Software platform for bayesian evolutionary analysis. Plos Computational Biology, 10(4), e1003537.
Burnham, K. P., & Anderson, D. R. (2004). Multimodel inference: understanding AIC and BIC in model selection. Sociol Methods Res, 33(2), 261–304.
Butler, M. A., & King, A. A. (2004). Phylogenetic comparative analysis: a modeling approach for adaptive evolution. The American Naturalist, 164, 683–695.
Chaudhary, A., Amin, O. M., Heckmann, R., & Singh, H. S. (2020). The molecular profile of Rhadinorhynchus dorsoventrospinosus Amin, Heckmann, and Ha 2011 (Acanthocephala: Rhadinorhynchidae) from Vietnam. J Para, 106(3), 418–427.
Church, S. H., Donoughe, S., de Medeiros, B. A., & Extavour, C. G. (2019). Insect egg size and shape evolve with ecology but not developmental rate. Nature, 571(7763), 58–62.
Deeming, D. C., & Ruta, M. (2014). Egg shape changes at the theropod–bird transition, and a morphometric study of amniote eggs. R Soc Open Sci, 1, 140311.
De Roos, A. M., Persson, L., & McCauley, E. (2003). The influence of size-dependent life‐history traits on the structure and dynamics of populations and communities. Ecology Letters, 6(5), 473–487.
Dezfuli, B. S. (1996). Cypria reptans (Crustacea: Ostracoda) as an intermediate host of Neoechinorhynchus rutili (Acanthocephala: Eoacanthocephala) in Italy. J Para, 82, 503–505.
Duursma, D. E., Gallagher, R. V., Price, J. J., & Griffith, S. C. (2018). Variation in avian egg shape and nest structure is explained by climatic conditions. Scientific Reports, 8(1), 1–10.
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.
Fayard, M., Dechaume-Moncharmont, F. X., Wattier, R., & Perrot‐Minnot, M. J. (2020). Magnitude and direction of parasite‐induced phenotypic alterations: a meta‐analysis in acanthocephalans. Biological Reviews, 95(5), 1233–1251.
Felsenstein, J. (1973). Maximum-likelihood estimation of evolutionary trees from continuous characters. American Journal Of Human Genetics, 25, 471–492.
Felsenstein, J. (1985). Phylogenies and the comparative method. The American Naturalist, 125, 1–15.
García-Varela, M., de León, G. P. P., Aznar, F. J., & Nadler, S. A. (2013). Phylogenetic relationship among genera of Polymorphidae (Acanthocephala), inferred from nuclear and mitochondrial gene sequences. Molecular Phylogenetics And Evolution, 68(2), 176–184.
Goeze, J. A. E. (1782). Versuch einer Naturgeschichte der Eingeweidewürmer thierischer körper (Vol. 1). gedruckt bey Philipp Pape, Fürstl. privilegirtem Buchdrucker.
George, P. V., & Nadakal, A. M. (1973). Studies on the life cycle of Pallisentis nagpurenis Bhalerao, 1931 (Pallisentidae; Acanthocephala) parasitic fish Ophiocephalus striatus (Bloch). Hydrobiologia, 42, 31–43.
Harmon, L. J., Losos, J. B., Davies, T. J., Gillespie, R. G., Gittleman, J. L., Jennings, B. W., Kozak, K. H., McPeek, M. A., Moreno-Roark, F., Near, T. J., & Purvis, A. (2010). Early bursts of body size and shape evolution are rare in comparative data. Evolution, 64(8), 2385–2396.
Harmon, L. J., Weir, J. T., Brock, C. D., Glor, R. E., & Challenger, W. (2008). GEIGER: investigating evolutionary radiations. Bioinformatics, 24, 129–131.
Jarecka, L. (1961). Morphological adaptions of tapeworm eggs and their importance in the life cycles. Acta Parasitol, 9, 409–426.
Kearn, G. C. (1986). The eggs of monogeneans. Advances In Parasitology, 25, 175–273.
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P., & Drummond, A. (2012). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649.
Kennedy, C. R. (2006). Ecology of the Acanthocephala. New York: Cambridge University Press.
Koehler, A. V., Brown, B., Poulin, R., Thieltges, D. W., & Fredensborg, B. L. (2012). Disentangling phylogenetic constraints from selective forces in the evolution of trematode transmission stages. Evolutionary Ecology, 26(6), 1497–1512.
Kostylev, N. (1924). Le genre Leptorhynchoides, nouveau genre d’Acanthocephale parasite des poissons. Annales de Parasitologie, 11, 214–215.
Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T., & Calcott, B. (2016). PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology And Evolution, 34, 772–773.
Linton, E. (1891). Notes on the entozoa of marine fishes with discriptions of new species, pt. III. Report of United States Commissioner of Fish and Fisheries, 16, 523–542.
Lühe, M. (1911) Acanthocephalen. Register der Acanthocephalen und parasitischen Plattwürmer geordnet nach ihern Wirten. Prof. Dr. Brauer, Die Süsswasserfauna Deutschlands, Eine Exkursionsfauna, Jena 16: 114 pp.
Marchand, B. (1984). A comparative ultrastructural study of the shell surrounding the mature acanthor larvae of 13 acanthocephalan species. J Para, 70, 886–901.
McConnell, C. J., Marcogliese, D. J., & Stacey, M. W. (1997). Settling rate and dispersal of sealworm eggs (Nematoda) determined using a revised protocol for myxozoan spores. J Para, 83(2), 203–206.
McDonald, M. E. (1988). Key to Acanthocephala reported in waterfowl. U. S. Fish and Wildlife Service, Resource Publication 173, Washington, D.C.
Müller, O. F. (1776). Zoologiae Danicae prodromus, seu, Animalium Daniae et Norvegiae indigenarum characteres, nomina, et synonyma imprimis popularium. Impensis auctoris.
Müller, O.F. (1780) Zoologiae Danicae seu Animalium Daniae et Norvegiae rariorum ac minus notorum. Icones, editae ab Othone Friderico Müller. Fasc.2. Havniae: Hallager, 2 p., Tab. 41–80.
Nikishin, V. P. (2001). The structure and formation of embryonic envelopes in acanthocephalans. Biological Bulletin, 28, 40–53.
Orme, D., Freckleton, R., Thomas, G., & Petzoldt, T. (2013). The caper package: comparative analysis of phylogenetics and evolution in R. R package version. 5:1–36.
Pellegrino, C. R. (1984). The role of desiccation pressures and surface area/volume relationships on seasonal zonation and size distribution of four intertidal decapod Crustacea from New Zealand: implications for adaptations on land. Crustaceana, 47(3), 251–268.
Peters, W., Taraschewski, H., & Latka, I. (1991). Comparative investigations of the morphology and chemical composition of the eggshells of Acanthocephala, I. Macracanthorhynchus hirudinaceus (Archiacanthocephala). Parasitology Research, 77, 542–549.
Pfenning, A. C. (2017). Egg morphology, dispersal, and transmission in acanthocephalan parasites: integrating phylogenetic and ecological approaches. MSc Thesis. College of Science and Health, DePaul University Chicago, Illinois, USA
Pfenning, A. C., & Sparkes, T. C. (2019). Egg fibrils and transmission in the acanthocephalan Acanthocephalus dirus. Parasitology Research, 118, 1225–1229.
R Core Team (2018). R: A language and environment for statistical computing.
Rambaut, A., Drummond, A. J., **e, D., Baele, G., & Suchard, M. A. (2018). Posterior summarization in bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67, 901–904.
Reading, K. L., & Backwell, P. R. (2007). Can beggars be choosers? Male mate choice in a fiddler crab. Animal Behaviour, 74(4), 867–872.
Revell, L. J. (2012). Phytools: an R package for phylogenetic comparative biology (and other things). Methods In Ecology And Evolution, 3(2), 217–223.
Sengupta, M. E., Thamsborg, S. M., Andersen, T. J., Olsen, A., & Dalsgaard, A. (2011). Sedimentation of helminth eggs in water. Water Research, 45, 4651–4660.
Smales, L. R. (2015). Acanthocephala. In A. Schmidt-Rhaesa (Ed.), Gastrotricha, Cycloneuralia, and Gnathifera (3 vol., pp. 317–335). Berlin: DeGruyter.
Smart, I. H. M. (1991). Egg shape in birds. In C. Deeming (Ed.), Egg incubation: its effects on embryonic development in birds and reptiles (pp. 101–116). New York: Cambridge University Press.
Stoddard, M. C., Yong, E. H., Akkaynak, D., Sheard, C., Tobias, J. A., & Mahadevan, L. (2017). Avian egg shape: form, function, and evolution. Science, 356, 1249–1254.
Takken, W., Klowden, M. J., & Chambers, G. M. (1998). Effect of body size on host seeking and blood meal utilization in Anopheles gambiae sensu stricto (Diptera: Culicidae): the disadvantage of being small. Journal Of Medical Entomology, 35(5), 639–645.
Taraschewski, H. (2000). Host-parasite interactions in Acanthocephala: a morphological approach. In J. R. Baker, R. Muller, & D. Rollinson (Eds.), Advances in parasitology (pp. 2–149). San Diego: Academic Press.
Taraschewski, H., & Peters, W. (1992). Comparative investigations of the morphology and chemical composition of the eggshells of Acanthocephala: II. Palaeacanthocephala. Parasitology Research, 78, 376–381.
Taraschewski, H., Peters, W., & Latka, I. (1992). Comparative investigations of the morphology and chemical composition of the eggshells of Acanthocephala: III. Eoacanthocephala. Parasitology Research, 78, 382–387.
Van Cleave, H. J. (1916). A revision of the genus Arhythmorhynchus with descriptions of two new species from North American birds. J Para, 2, 167–174.
Van Cleave, H. J. (1918). The Acanthocephala of North American Birds. Trans Am Microsc Soc, 37, 19–47.
Van Cleave, H. J. (1919). Acanthocephala from the Illinois River, with descriptions of species and a synopsis of the family Neoechinorhynchidae. Bull Ill Nat Hist Surv, 13, 225–257.
Van Cleave, H. J. (1931). New Acanthocephala from fishes of Mississippi and a taxonomic reconsideration of forms with unusual numbers of cement glands. Transactions of the American Microscopical Society, 50(4), 348–363.
Van Cleave, H. J., & Townsend, L. H. (1936). On the assignment of Echinorhynchus dims to the genus Acanthocephalus. Proc. Helminthol. Soc. Wash., 3, 63.
Verweyen, L., Klimpel, S., & Palm, H. W. (2011). Molecular phylogeny of the Acanthocephala (class Palaeacanthocephala) with a paraphyletic assemblage of the orders Polymorphida and Echinorhynchida. PLoS One, 6(12), e28285.
Wongkham, W., & Whitfield, P. J. (2004). Pallisentis rexus from the Chiang Mai Basin, Thailand: ultrastructural studies on egg envelope development and the mechanism of egg expansion. Journal Of Helminthology, 78, 77–85.
Woodward, G., Ebenman, B., Emmerson, M., Montoya, J. M., Olesen, J. M., Valido, A., & Warren, P. H. (2005). Body size in ecological networks. Trends In Ecology & Evolution, 20(7), 402–409.
Acknowledgements
Funding was provided by the Department of Biological Sciences, College of Health and Science, DePaul University, Chicago, IL. This research is part of a thesis to fulfill the requirements for the MSc Program at DePaul University.
Funding
No funding was received for conducting this study.
Author information
Authors and Affiliations
Contributions
Both authors designed the study; A.P.B. preformed the analysis; both authors analyzed the output. A.P.B. wrote the first draft of the manuscript and both authors contributed to the revisions.
Corresponding author
Ethics declarations
Conflicts of interest/Competing Interests
The authors have no competing interests.
Ethics Approval
This data in this study was collected from the published literature, no ethical approval is required.
Consent to Participate
This research did not involve human subjects.
Consent for publication
This research did not involve human subjects.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Pfenning-Butterworth, A.C., Sparkes, T.C. Evolutionary History and host Ecology Determine Acanthocephalan Egg Shape. Evol Biol 50, 137–145 (2023). https://doi.org/10.1007/s11692-022-09595-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11692-022-09595-9