Skip to main content Accessibility help
×
Home

Estimating effective population size for a cestode parasite infecting three-spined sticklebacks

  • Hannah M. Strobel (a1) (a2), Sara J. Hays (a1) (a3), Kristine N. Moody (a4) (a5), Michael J. Blum (a1) (a4) (a5) and David C. Heins (a1)...

Abstract

Remarkably few attempts have been made to estimate contemporary effective population size (Ne) for parasitic species, despite the valuable perspectives it can offer on the tempo and pace of parasite evolution as well as coevolutionary dynamics of host–parasite interactions. In this study, we utilized multi-locus microsatellite data to derive single-sample and temporal estimates of contemporary Ne for a cestode parasite (Schistocephalus solidus) as well as three-spined stickleback hosts (Gasterosteus aculeatus) in lakes across Alaska. Consistent with prior studies, both approaches recovered small and highly variable estimates of parasite and host Ne. We also found that estimates of host Ne and parasite Ne were sensitive to assumptions about population genetic structure and connectivity. And, while prior work on the stickleback–cestode system indicates that physiographic factors external to stickleback hosts largely govern genetic variation in S. solidus, our findings indicate that stickleback host attributes and factors internal to the host – namely body length, genetic diversity and infection – shape contemporary Ne of cestode parasites.

Copyright

Corresponding author

Author for correspondence: Hannah M. Strobel, E-mail: hannahmstrobel@gmail.com

References

Hide All
Aeschlimann, PB, Häberli, MA, Reusch, TBH, Boehm, T and Milinski, M (2003) Female stickelbacks Gasterosteus aculeatus use self-reference to optimize MHC allele number during mate selection. Behavioral Ecology and Sociobiology 54, 119126.
Anderson, TJC, Hauhold, B, Williams, JT, Estrada-Franco, JG, Richardson, L., Mollinedo, R, Brockarie, M, Mokili, J, Mharakurwa, S, French, N, Whitworth, J, Velez, ID, Brockman, AH, Nosten, F, Ferreira, MU and Day, KP (2000) Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Molecular Biology and Evolution 17, 14671482.
Araguas, RM, Vidal, O, Pla, C and Sanz, N (2012) High genetic diversity of the endangered Iberian three-spined stickleback (Gasterosteus aculeatus) at the Mediterranean edge of its range. Freshwater Biology 57, 143154.
Baalsrud, HT, Sæther, B-K, Hagen, IJ, Myhre, AM, Ringsby, TH, Pärn, H and Jensen, H (2014) Effects of population characteristics and structure on estimates of effective population size in a house sparrow metapopulation. Molecular Ecology 23, 26532668.
Bagamian, KH, Heins, DC and Baker, JA (2004) Body condition and reproductive capacity of three-spined stickleback infected with the cestode Schistocephalus solidus. Journal of Fish Biology 64, 15681576.
Baker, JA, Heins, DC, Foster, SA and King, RW (2008) An overview of life-history variation in female three-spined stickleback. Behaviour 145, 579602.
Barber, I (2013) Sticklebacks as model hosts in ecological and evolutionary parasitology. Trends in Parasitology 29, 556566.
Barber, I and Huntingford, FA (1995) The effect of Schistocephalus solidus (Cestoda: Pseudophyllidea) on the foraging and shoaling behavior of three-spined sticklebacks, Gasterosteus aculeatus. Behaviour 132, 12231240.
Blouin, MS, Dame, JB, Tarrant, CA and Courtney, CH (1992) Unusual population genetics of a parasite nematode: mtDNA variation within and among populations. Evolution 46, 470476.
Boulinier, T, Ives, AR and Danchin, E (1996) Measuring aggregation of parasites at different host population levels. Parasitology 112, 581587.
Caldera, EJ and Bolnick, DI (2008) Effects of colonization and landscape structure on genetic variation within and among three-spined stickleback (Gasterosteus aculeatus) populations in a single watershed. Evolutionary Ecology Research 10, 575598.
Crellen, T, Allan, F, David, S, Durrant, C, Huckvale, T, Holroyd, N, Emery, AM, Rollinson, D, Aanensen, DM, Berriman, M, Webster, JP and Cotton, JA (2016) Whole genome resequencing of the human parasite Schistosoma mansoni reveals population history and effects of selection. Scientific Reports 6, 20954.
Criscione, CD (2013) Genetic epidemiology of Ascaris: cross-transmission between humans and pigs, focal transmission, and effective population size. In Holland, CV (ed), Ascaris: The Neglected Parasite. London, UK: Academic Press, pp. 203230.
Criscione, CD (2016) History of microevolutionary thought in parasitology: the integration of molecular population genetics. In Janovy, J and Esch, GW (eds), A Century of Parasitology: Discoveries, Ideas and Lessons Learned by Scientists who Have Published in the Journal of Parasitology, 1914–2014. Chichester, UK: John Wiley & Sons, Ltd, pp. 93109.
Criscione, CD and Blouin, MS (2005) Effective sizes of macroparasite populations: a conceptual model. TRENDS in Parasitology 21, 212217.
Criscione, CD, Poulin, R and Blouin, MS (2005) Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Molecular Ecology 14, 22472257.
DeWoody, JA and Avise, JC (2000) Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. Journal of Fish Biology 56, 461473.
Dieringer, D and Schlštterer (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Molecular Ecology Notes 3, 167169.
Do, C, Waples, RS, Peel, D, Macbeth, GM, Tillett, BJ and Ovenden, JR (2014) Neestimator V2: re-implementation of software for the estimation of contemporary effective population size (N e) from genetic data. Molecular Ecology Resources 14, 209214.
Doña, J, Moreno-Garcia, M, Criscione, CD, Serrano, D and Jovani, R (2015) Species mtDNA genetic diversity explained by infrapopulation size in a host-symbiont system. Ecology and Evolution 5, 58015809.
Excoffier, L and Lischer, HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564567.
Frommen, JG, Luz, C, Mazzi, D and Bakker, TCM (2008) Inbreeding depression affects fertilization success and survival but not breeding coloration in three-spined sticklebacks. Behaviour 145, 425441.
Gagne, RB, Hogan, DJ, Pracheil, BM, McIntyre, PB, Hain, EF, Gilliam, JF and Blum, MJ (2015) Spread of an introduced parasite across the Hawaiian archipelago independent of its introduced host. Freshwater Biology 60, 311322.
Gagne, RB, Tinker, TM, Gustafson, KD, Ralls, K, Larson, S, Tarjan, LM, Miller, MA and Ernest, HB (2018) Measures of effective population size in sea otters reveal special considerations for wide-ranging species. Evolutionary Applications 11, 112.
Gower, CM, Gouvras, AN, Lamberton, PHL, Deol, A, Shrivastava, J, Mutombo, PN, Mbuh, JV, Norton, AJ, Webster, BL, Stothard, JR, Garba, A, Lamine, MS, Kariuki, C, Lange, CN, Mkoji, GM, Kabatereine, NB, Gabrielli, AF, Rudge, JW, Fenwick, A, Sacko, M, Dembelé, R, Lwambo, NJS, Tchuem Tchuenté, L-A, Rollinson, D and Webster, JP (2013) Population genetic structure of Schistosoma mansoni and Schistosoma haematobium from across six sub-Saharan African countries: implications for epidemiology, evolution and control. Acta Tropica 128, 261274.
Greenbank, J and Nelson, PR (1959) Life history of the three-spined stickleback Gasterosteus aculeatus Linnaeus in Karluk Lake and Bare Lake, Kodiak Island, Alaska. Fishery Bulletin of the Fish and Wildlife Service 59, 537559.
Hare, MP, Nunney, L, Schwartz, MK, Ruzzante, DE, Burford, M, Waples, RS, Ruegg, K and Palstra, F (2011) Understanding and estimating effective population size for practical application in marine species management. Conservation Biology 25, 438449.
Harmon, L. and Braude, S (2010) Conservation of small populations: effective population sizes, inbreeding, and the 50/500 rule. In Braude, S and Low, SB (eds). An Introduction to Methods and Models in Ecology and Conservation Biology. Princeton, NJ, USA: Princeton University Press, pp. 125138.
Hatcher, MJ, Dick, JTA and Dunn, AM (2012) Diverse effects of parasites in ecosystems: linking interdependent processes. Frontiers in Ecology and the Environment 10, 186194.
Hedrick, P (2011) Genetics of Populations, 4th Edn. Massachusetts: Jones & Bartlett Learning Press.
Heins, DC and Baker, JA (2008) The stickleback–Schistocephalus host–parasite system as a model for understanding the effect of a macroparasite on host reproduction. Behaviour 145, 625645.
Heins, DC, Singer, SS and Baker, JA (1999) Virulence of the cestode Schistocephalus solidus and reproduction in infected three-spined stickleback, Gasterosteus aculeatus. Canadian Journal of Zoology 77, 19671974.
Heins, DC, Baker, JA and Martin, HC (2002) The ‘crowding effect’ in the cestode Schistocephalus solidus: density-dependent effects on plerocercoid size and infectivity. Journal of Parasitology 88, 302307.
Heins, DC, Birden, EL and Baker, JA (2010) Host mortality and variability in epizootics of Schistocephalus solidus infecting the three-spined stickleback, Gasterosteus aculeatus. Parasitology 137, 16811686.
Heins, DC, Eidam, DM and Baker, JA (2016) Timing of infections in the threespine stickleback (Gasterosteus aculeatus) by Schistocephalus solidus in Alaska. Journal of Parasitology 102, 286289.
Hill, WG (1981) Estimation of effective population size from data on linkage disequilibrium. Genetics Research 38, 209216.
Hughes, AL and Verra, F (2001) Very large long-term effective population size in the virulent human malaria parasite Plasmodium falciparum. Proceedings of the Royal Society B 268, 18551860.
Huyse, T, Poulin, R and Théron, A (2005) Speciation in parasites: a population genetics approach. Trends in Parasitology 21, 469475.
Jan, P-L, Cracianne, C, Fournet, S, Olivier, E, Arnaud, J-F, Porte, C, Bardou-Valette, S, Denis, M-C and Petit, EJ (2016) Temporal sampling helps unravel the genetic structure of naturally occurring populations of a phytoparasitic nematode. 1. Insights from the estimation of effective population sizes. Evolutionary applications 9, 489501.
Jensen, JD and Bachtrog, D (2011) Characterizing the influence of effective population size on the rate of adaptation: Gillespie's Darwin domain. Genome biology and evolution 3, 687701.
Joy, DA, Feng, X, Mu, J, Furuya, T, Chotivanich, K, Krettli, AU, Ho, M, Wang, A, White, NJ, Suh, E, Beerli, P and Su, X (2003) Early origin and recent expansion of Plasmodium falciparum. Science 300, 318321.
Kalbe, M, Eizaguirre, C, Scharsack, JP and Jakobsen, PJ (2016) Reciprocal cross infection of sticklebacks with the diphyllobothriidean cestode Schistocephalus solidus reveals consistent population differences in parasite growth and host resistance. Parasites & Vectors 9, 130.
Kaunisto, KM, Viitaniemi, HM, Leder, EH and Suhonen, J (2013) Association between host's genetic diversity and parasite burden in damselflies. Journal of Evolutionary Biology 26, 17841789.
Koffi, M, de Meeûs, T, Bucheton, B, Solano, P, Camara, M, Kaba, D, Cuny, G, Ayala, FJ and Jamonneau, V (2009) Population genetics of Trypanosoma brucei gambiense, the agent of sleeping sickness in Western Africa. PNAS 106, 209214.
Kurtz, J, Kalbe, M, Aeschlimann, PB, Häberli, MA, Wegner, KM, Reusch, TB and Milinski, M (2004) Major histocompatibility complex diversity influences parasite resistance and innate immunity in sticklebacks. Proceedings of the Royal Society of London B: Biological Sciences 271, 197204.
Legendre, P (2008) Studying beta diversity: ecological variation partitioning by multiple regression and canonical analysis. Journal of Plant Ecology 1, 38.
Mäkinen, HS, Cano, JM and Merilä, J (2006) Genetic relationships among marine and freshwater populations of the European three-spined stickleback (Gasterosteus aculeatus) revealed by microsatellites. Molecular Ecology 15, 15191534.
Marcogliese, DJ (2004) Parasites: small players with crucial roles in the ecological theater. EcoHealth 1, 151164.
McPhail, JD and Peacock, SD (1983) Some effects of the cestode (Schistocephalus solidus) on reproduction in the three-spined stickleback (Gasterosteus aculeatus): evolutionary aspects of a host–parasite interaction. Canadian Journal of Zoology 61, 901908.
Morand, S, Pointier, J, Borel, G and Theron, A (1993) Pairing probability of schistosomes related to their distribution among the host population. Ecology 74, 24442449.
Ness, JH and Foster, SA (1999) Parasite-associated phenotype modifications in three-spined stickleback. Oikos 85, 127134.
Nishimura, N, Heins, DC, Andersen, RO, Barber, I and Cresco, WA (2011) Distinct lineages of Schistocephalus solidus parasites in three-spined and ninespine stickleback hosts revealed by DNA sequence analysis. PLoS ONE 6, e22505.
Nkhoma, SC, Nair, S, Al-Saai, S, Ashley, E, McGready, R, Phyo, AP, Nosten, F and Anderson, TJC (2013) Population genetic correlates of declining transmission in a human pathogen. Molecular Ecology 22, 273285.
Oksanen, J, Blanchet, FG, Friendly, M, Kindt, R, Legendre, P, McGlinn, D, Minchin, PR, O'Hara, RB, Simpson, GL, Solymos, P, Stevens, MHH, Szoecs, E and Wagner, H (2016) vegan: Community ecology package. R package version 2.4-1. Available at https://CRAN.R-project.org/package=vegan.
Papkou, A, Gokhale, CS, Traulsen, A and Schulenburg, H (2016) Host–parasite coevolution: why changing population size matters. Zoology 119, 330338.
Pascoe, D and Mattey, D (1977) Dietary stress in parasitized and non-parasitized Gasterosteus aculeatus L. Zeitschrift für Parasitenkunde 51, 179186.
Penczykowski, RM, Laine, A-L and Koskella, B (2016) Understanding the ecology and evolution of host–parasite interactions across scales. Evolutionary Applications 9, 3752.
Peres-Neto, PR and Legendre, P (2010) Estimating and controlling or spatial structure in the study of ecological communities. Global Ecology and Biogeography 19, 174184.
Poulin, R (2007) Evolutionary Ecology of Parasites. Princeton, NJ: Princeton University Press.
Poulin, R (2013) Explaining variability in parasite aggregation levels among host samples. Parasitology 140, 541546.
Poulin, R and Morand, S (2000) The diversity of parasites. The Quarterly Review of Biology 75, 277293.
Prugnolle, F, Liu, H, de Meeûs, T and Balloux, F (2005) Population genetics of complex life-cycle parasites: an illustration with trematodes. International Journal for Parasitology 35, 255263.
Rao, CR (1964) The use and interpretation of principal component analysis in applied research. Sankhyā: The Indian Journal of Statistics, Series A 26, 329358.
R Core Team (2016) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. Available at http://www.R-project.org.
Read, CP (1951) The ‘crowding effect’ in tapeworm infections. The Journal of Parasitology 37, 174178.
Reusch, TBH, Wegner, KM and Kalbe, M (2001) Rapid genetic divergence in postglacial populations of three-spined stickleback (Gasterosteus aculeatus): the role of habitat type, drainage and geographical proximity. Molecular Ecology 10, 24352445.
Robinson, JD and Moyer, GR (2013) Linkage disequilibrium and effective population size when generations overlap. Evolutionary Applications 6, 290302.
Saito, T and Nakano, S (1999) Reproductive-timing-dependent alternation of offspring life histories in female three-spined sticklebacks. Canadian Journal of Zoology 77, 13141321.
Sisya, TJ, Kamn'gona, RM, Vareta, JA, Fulakeza, JM, Mukaka, MFJ, Seydel, KB, Laufer, MK, Taylor, TE and Nkhoma, SC (2015) Subtle changes in Plasmodium falciparum infection complexity following enhanced intervention in Malawi. Acta Tropica 142, 108114.
Smyth, JD (1946) Studies on tapeworm physiology – I. The cultivation of Schistocephalus solidus in vitro. Journal of Experimental Biology 23, 4770.
Smyth, J (1962) Introduction to Animal Parasitology. Springfield, IL: Charles C Thomas.
Sprehn, CG, Blum, MJ, Quinn, TP and Heins, DC (2015) Landscape genetics of Schistocephalus solidus parasites in three-spined stickleback (Gasterosteus aculeatus) from Alaska. PLoS ONE 10, e0122307.
Steinauer, ML, Christie, MR, Blouin, MS, Agola, LE, Mwangi, IN, Maina, GM, Mutuku, MW, Kinuthia, JM, Mkoji, GM and Loker, ES (2013) Non-invasive sampling of Schistosomes from humans requires correcting for family structure. PLoS Neglected Tropical Diseases 7, e2456.
Strobel, HM, Alda, F, Sprehn, CG, Blum, MJ and Heins, DC (2016) Geographic and host-mediated population genetic structure in a cestode parasite of the three-spined stickleback. Biological Journal of the Linnean Society 119, 381396.
van Baalen, M and Beekman, M (2006) The costs and benefits of genetic heterogeneity in resistance against parasites and social insects. The American Naturalist 167, 568577.
Van Oosterhout, C, Hutchinson, WF, Wills, DPM and Shipley, P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535538.
von Hippel, FA (2008) Conservation of three-spined and ninespine stickleback radiations in the cook inlet basin, Alaska. Behaviour 145, 693724.
Waits, ER, Bagley, MJ, Blum, MJ, McCormick, FH and Lazorchak, JM (2008) Source–sink dynamics sustain central stonerollers (Campostoma anomalum) in a heavily urbanized catchment. Freshwater Biology 53, 20612075.
Wang, J and Whitlock, MC (2003) Estimating effective population size and migration rates from genetic samples over space and time. Genetics 163, 429446.
Waples, RS and Do, C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Molecular Ecology Resources 8, 753756.
Waples, RS and Do, C (2010) Linkage disequilibrium estimates of contemporary N e using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evolutionary Applications 3, 244262.
Waples, RS and Yokota, M (2007) Temporal estimates of effective population size in species with overlapping generations. Genetics 175, 219233.
Waples, RS, Antao, T and Luikart, G (2014) Effects of overlapping generations on linkage disequilibrium estimates of effective population size. Genetics 197, 769780.
Weber, JN, Steinel, NC, Shim, KC and Bolnick, DI (2017) Recent evolution of extreme cestode growth suppression by a vertebrate host. Proceedings of the National Academy of Sciences 114, 65756580.
Woolhouse, MEJ, Webster, JP, Domingo, E, Charlesworth, B and Levin, BR (2002) Biological and biomedical implications of co-evolution of pathogens and their hosts. Nature Genetics 32, 569577.
Wright, S (1931) Evolution in Mendelian populations. Genetics 16, 97159.
Wright, S (1938) Size of population and breeding structure in relation to evolution. Science 87, 430431.

Keywords

Type Description Title
WORD
Supplementary materials

Strobel et al. supplementary material
Tables S1-S3

 Word (47 KB)
47 KB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed