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Spatial and genetic structure of directly-transmitted parasites reflects the distribution of their specific amphibian hosts

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Population Ecology

Abstract

Parasite distributions depend on the local environment in which host infection occurs, and the surrounding landscape over which hosts move and transport their parasites. Although host and landscape effects on parasite prevalence and spatial distribution are difficult to observe directly, estimation of such relationships is necessary for understanding the spread of infections and parasite–habitat associations. Although parasite distributions are necessarily nested within host distributions, direct environmental influences on local infection or parasite effects on host dispersal could lead to distinct landscape or habitat relationships relative to their hosts. Our aim was to determine parasite spatial structure across a contiguous prairie by statistical modeling of parasite–landscape relationships combined with analysis of population genetic structure. We sampled northern leopard frogs (Lithobates pipiens) and wood frogs (L. sylvaticus) for host-specific lung nematodes (Rhabdias ranae and R. bakeri; respectively) across the Sheyenne National Grassland in southeastern North Dakota and developed primers for 13 microsatellite loci for Rhabdias. The two Rhabdias species exhibited different correlations with landscape characteristics that conformed with that of their hosts, indicating transmission is driven by host ecology, probably density, and not directly by the environment. There was evidence for localized, patchy spatial genetic structure, but no broader-scale geographic patterns, indicating no barriers to host and parasite dispersal. Nematodes cohabitating in an individual frog were most genetically similar. Worms within the same wetland were also genetically similar, indicating localized transmission and resulting wetland-scale patchiness are not completely obscured by broad-scale host–parasite dispersal. Beyond individual wetlands, we found no evidence of genetic isolation-by-distance or patchiness at the landscape-scale.

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References

  • Alho JS, Valimaki K, Merila J (2010) Rhh: An R extension for estimating multilocus heterozygosity and heterozygosity–heterozygosity correlation. Mol Ecol Resour 10:720–722

    Article  PubMed  Google Scholar 

  • Amos W, Wilmer JW, Fullard K, Burg T, Croxall J, Bloch D, Coulson T (2001) The influence of parental relatedness on reproductive success. Proc R Soc Lond B 268:2021–2027

    Article  CAS  Google Scholar 

  • Anderson R, Gordon D (1982) Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85:373–398

    Article  PubMed  Google Scholar 

  • Anderson TJC, Romero-Abal ME, Jaenike J (1995) Mitochondrial DNA and Ascaris microepidemiology: The composition of parasite populations from individual hosts, families and villages. Parasitology 110:221–229

    Article  PubMed  Google Scholar 

  • Anderson TJC, Blouin MS, Beech RN (1998) Population biology of parasitic nematodes: applications of genetic markers. Adv Parasitol 41:219–283

    Article  PubMed  CAS  Google Scholar 

  • Archie EA, Ezenwa VO (2011) Population genetic structure and history of a generalist parasite infecting multiple sympatric host species. Int J Parasitol 41:89–98

    Article  PubMed  Google Scholar 

  • Archie EA, Luikart G, Ezenwa VO (2009) Infecting epidemiology with genetics: a new frontier in disease ecology. Trends Ecol Evol 24:21–30

    Article  PubMed  Google Scholar 

  • Arneberg P, Skorping A, Grenfell B, Read AF (1998) Host densities as determinants of abundance in parasite communities. Proc R Soc Lond B 265:1283–1289

    Article  Google Scholar 

  • Baker M (1979) The free-living and parasitic development of Rhabdias spp. (Nematoda: Rhabdiasidae) in amphibians. Can J Zool 57:161–178

    Article  Google Scholar 

  • Bartoń K (2016) MuMIn: model selection and model averaging based on information criteria (AICc and alike) R package version 1.15.6. Comprehensive R Archive Network repository. https://cran.r-project.org/web/packages/MuMIn/MuMIn.pdf. Accessed 21 Aug 2017

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Beaupre SJ, Jacobson ER, Lillywhite HB, Zamudio K (2004) Guidelines for the use of live amphibians and reptiles in field and laboratory research, 2nd edn. American Society of Ichthyologists and Herpetologists, Kansas

    Google Scholar 

  • Berven KA, Grudzien TA (1990) Dispersal in the wood frog (Rana sylvatica): implications for genetic population structure. Evolution 44:2047–2056

    PubMed  Google Scholar 

  • Biek R, Real LA (2010) The landscape genetics of infectious disease emergence and spread. Mol Ecol 19:3515–3531

    Article  PubMed  PubMed Central  Google Scholar 

  • Blouin MS, Dame JB, Tarrant CA, Courtney CH (1992) Unusual population genetics of a parasitic nematode: MtDNA varaition within and among populations. Evolution 46:470–476

    Article  PubMed  Google Scholar 

  • Blouin MS, Yowell CA, Courtney CH, Dame JB (1995) Host movement and the genetic structure of populations of parasitic nematodes. Genetics 141:1007–1014

    PubMed  PubMed Central  CAS  Google Scholar 

  • Bolek MG, Stigge HA, Gustafson KD (2016) The iron wheel of parasite life cycles: then and now! In: Janovy J Jr, Esch GW (eds) A century of parasitology: discoveries, ideas and lessons learned by scientists who published in the journal of parasitology, 1914–2014. John Wiley, London, pp 131–147

    Chapter  Google Scholar 

  • Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135

    Article  PubMed  Google Scholar 

  • Brooker S, Michael E (2000) The potential of geographical information systems and remote sensing in the epidemiology and control of human helminth infections. Adv Parasitol 47:245–288

    Article  PubMed  CAS  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583

    Article  PubMed  CAS  Google Scholar 

  • Chybicki IJ, Burczyk J (2009) Simultaneous estimation of null alleles and inbreeding coefficients. J Hered 100:106–113

    Article  PubMed  CAS  Google Scholar 

  • Criscione CD, Poulin R, Blouin MS (2005) Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Mol Ecol 14:2247–2257

    Article  PubMed  CAS  Google Scholar 

  • Criscione CD, Anderson JD, Sudimack D, Subedi J, Upadhayay RP, Jha B, Williams KD, Williams-Blangero S, Anderson TJ (2010) Landscape genetics reveals focal transmission of a human macroparasite. Plos Negl Trop Dis 4:e665

    Article  PubMed  PubMed Central  Google Scholar 

  • Cunningham MA, Johnson DH (2006) Proximate and landscape factors influence grassland bird distributions. Ecol Appl 16:1062–1075

    Article  PubMed  Google Scholar 

  • de la Cruz Rot M (2005) Improving the presentation of results of logistic regression with R. ESA Bull 86:41–48

    Google Scholar 

  • Dole JW (1968) Homing in leopard frogs, Rana pipiens. Ecology 49:386–399

    Article  Google Scholar 

  • Durand E, Jay F, Gaggiotti OE, François O (2009) Spatial inference of admixture proportions and secondary contact zones. Mol Biol Evol 26:1963–1973

    Article  PubMed  CAS  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  PubMed  CAS  Google Scholar 

  • Faircloth BC (2008) MSATCOMMANDER: detection of microsatellite repeat arrays and automated, locus-specific primer design. Mol Ecol Resour 8:92–94

    Article  PubMed  CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed  PubMed Central  CAS  Google Scholar 

  • Funk WC, Blouin MS, Corn PS, Maxell BA, Pilliod DS, Amish S, Allendord FW (2005) Population structure of Columbia spotted frogs (Rana luteiventris) is strongly affected by the landscape. Mol Ecol 14:483–496

    Article  PubMed  CAS  Google Scholar 

  • Gendron AD, Marcogliese DJ, Barbeau S, Christin MS, Brousseau P, Ruby S, Cyr D, Fournier M (2003) Exposure of leopard frogs to a pesticide mixture affects life history characteristics of the lungworm Rhabdias ranae. Oecologia 135:469–476

    Article  PubMed  CAS  Google Scholar 

  • Goater CP, Ward PI (1992) Negative effects of Rhabdias bufonis (Nematoda) on the growth and survival of toads (Bufo bufo). Oecologia 89:161–165

    Article  PubMed  CAS  Google Scholar 

  • Goldberg SR, Bursey CR, McKinnell RG, Tan IS (2001) Helminths of northern Leopard frogs, Rana pipiens (Ranidae), from North Dakota and South Dakota. West N Am Nat 61:248–251

    Google Scholar 

  • Goudet J (1995) FSTAT (version 1.2): a computer program to calculate. F stat J Hered 86:485–486

    Article  Google Scholar 

  • Gustafson KD, Newman RA (2016) Multiscale occupancy patterns of anurans in prairie wetlands. Herpetologica 72:293–302

    Article  Google Scholar 

  • Gustafson KD, Newman RA, Tkach VV (2013) Effects of host species and life stage on the helminth communities of sympatric Northern Leopard Frogs (Lithobates pipiens) and Wood Frogs (Lithobates sylvaticus) in the Sheyenne National Grasslands, North Dakota. J Parasitol 99:587–594

    Article  PubMed  Google Scholar 

  • Gustafson KD, Newman RA, Pulis EE, Cabarle KC (2015) A Skeletochronological assessment of age–parasitism relationships in wood frogs (Lithobates sylvaticus). J Herpetol 49:122–130

    Article  Google Scholar 

  • Gustafson KD, Belden JB, Bolek MG (2016) Atrazine reduces the transmission of an amphibian trematode by altering snail and ostracod host–parasite interactions. Parasitol Res 115:1583–1594

    Article  PubMed  Google Scholar 

  • Hatcher MJ, Dick JTA, Dunn AM (2012) Diverse effects of parasites in ecosystems: linking interdependent processes. Front Ecol Environ 10:186–194

    Article  Google Scholar 

  • Hedrick PW (2011) Genetics of populations, 4th edn. Jones & Bartlett Learning, London

    Google Scholar 

  • Hudson ME (2008) Sequencing breakthroughs for genomic ecology and evolutionary biology. Mol Ecol Resour 8:3–17

    Article  PubMed  CAS  Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    Article  PubMed  CAS  Google Scholar 

  • Kelehear C, Webb J, Shine R (2009) Rhabdias pseudosphaerocephala infection in Bufo marinus: Lung nematodes reduce viability of metamorph cane toads. Parasitology 136:919–927

    Article  PubMed  CAS  Google Scholar 

  • King KC, McLaughlin JD, Gendron AD, Pauli BD, Giroux I, Rondeau B, Boily M, Juneau P, Marcogliese DJ (2007) Impacts of agriculture on the parasite communities of northern leopard frogs (Rana pipiens) in southern Quebec. Can Parasitol 134:2063–2080

    CAS  Google Scholar 

  • King KC, Mclaughlin JD, Boily M, Marcogliese DJ (2010) Effects of agricultural landscape and pesticides on parasitism in native bullfrogs. Biol Conserv 143:302–310

    Article  Google Scholar 

  • Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) CLUMPAK: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kuzmin Y (2013) Review of Rhabdiasidae (Nematoda) from the Holarctic. Zootaxa 3639:1–76

    Article  PubMed  Google Scholar 

  • Lampert KP, Rand AS, Mueller UG, Ryan MJ (2003) Fine-scale genetic pattern and evidence for sex-biased dispersal in the túngara frog, Physalaemus pustulosus. Mol Ecol 12:3325–3334

    Article  PubMed  CAS  Google Scholar 

  • Langford GJ, Janovy J Jr (2009) Comparative life cycles and life histories of north american Rhabdias spp. (nematoda: Rhabdiasidae): lungworms from snakes and anurans. J Parasitol 95:1145–1155

    Article  PubMed  Google Scholar 

  • Langford GJ, Janovy J Jr (2013) Host specificity of North American Rhabdias spp. (Nematoda: Rhabdiasidae): Combining field data and experimental infections with a molecular phylogeny. J Parasitol 99:277–286

    Article  PubMed  CAS  Google Scholar 

  • Langford GJ, Janovy J Jr (2016) Ecological factors responsible for the geographic distribution of Rhabdias joaquinensis: Where do lungworms infect anurans in nature? Parasitol Res 115:1305–1313

    Article  PubMed  Google Scholar 

  • Lynch M, Ritland K (1999) Estimation of pairwise relatedness with molecular markers. Genetics 152:1753–1766

    PubMed  PubMed Central  CAS  Google Scholar 

  • McCoy KD, Boulinier T, Tirard C, Michalakis Y (2003) Host-dependent genetic structure of parasite populations: differential dispersal of seabird tick host races. Evolution 57:288–296

    Article  PubMed  Google Scholar 

  • Nadler SA (1995) Microevolution and the genetic structure of parasite populations. J Parasitol 81:395–403

    Article  PubMed  CAS  Google Scholar 

  • Ostfeld RS, Glass GE, Keesing F (2005) Spatial epidemiology: an emerging (or re-emerging) discipline. Trends Ecol Evol 20:328–336

    Article  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Price PW (1980) Evolutionary biology of parasites, 15th edn. Princeton University Press, Princeton

    Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  PubMed Central  CAS  Google Scholar 

  • Prugnolle F, Liu H, De Meeûs T, Balloux F (2005) Population genetics of complex life-cycle parasites: an illustration with trematodes. Int J Parasitol 35:255–263

    Article  PubMed  Google Scholar 

  • Prunier JG, Kaufmann B, Fenet S, Picard D, Pompanon F, Joly P, Lena JP (2013) Optimizing the trade-off between spatial and genetic sampling efforts in patchy populations: towards a better assessment of functional connectivity using an individual-based sampling scheme. Mol Ecol 22:5516–5530

    Article  PubMed  CAS  Google Scholar 

  • Pulis EE, Tkach VV, Newman RA (2011) Helminth parasites of the wood frog, Lithobates sylvaticus, in prairie pothole wetlands of the Northern Great Plains. Wetlands 31:1–11

    Article  Google Scholar 

  • Rosenberg MS, Anderson CD (2011) PASSaGE: pattern analysis, spatial statistics and geographic exegesis. Version 2. Methods Ecol Evol 2:229–232

    Article  Google Scholar 

  • Rousset F (2000) Genetic differentiation between individuals. J Evol Biol 13:58–62

    Article  Google Scholar 

  • Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Method Mol Biol 132:365–386

    CAS  Google Scholar 

  • Schwartz MK, McKelvey KS (2009) Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conserv Genet 10:441–452

    Article  Google Scholar 

  • Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629

    Article  PubMed  Google Scholar 

  • Shutler D, Gendron AD, Rondeau M, Marcogliese DJ (2014) Nematode parasites and leukocyte profiles of northern leopard frogs, Rana pipiens: location, location, location. Can J Zool 93:41–49

    Article  Google Scholar 

  • Smith MA, Green DM (2005) Dispersal and the metapopulation paradigm in amphibian ecology and conservation: are all amphibian populations metapopulations? Ecography 28:110–128

    Article  Google Scholar 

  • Thrall PH, Burdon JJ (1997) Host–pathogen dynamics in a metapopulation context: the ecological and evolutionary consequences of being spatial. J Ecol 85:743–753

    Article  Google Scholar 

  • Thrall PH, Hochberg ME, Burdon JJ, Bever JD (2007) Coevolution of symbiotic mutualists and parasites in a community context. Trends Ecol Evol 22:120–126

    Article  PubMed  Google Scholar 

  • Tkach VV, Kuzmin Y, Pulis EE (2006) A new species of Rhabdias from lungs of the wood frog, Rana sylvatica, in North America: the last sibling of Rhabdias ranae? J Parasitol 92:631–636

    Article  PubMed  Google Scholar 

  • Tkach VV, Kuzmin Y, Snyder SD (2014) Molecular insight into systematics, host associations, life cycles and geographic distribution of the nematode family Rhabdiasidae. Int J Parasitol 44:273–284

    Article  PubMed  Google Scholar 

  • Watts PC, Rousset F, Saccheri IJ, Leblois R, Kemp SJ, Thompson DJ (2007) Compatible genetic and ecological estimates of dispersal rates in insect (Coenagrion mercuriale: Odonata: Zygoptera) populations: analysis of ‘neighbourhood size’ using a more precise estimator. Mol Ecol 16:737–751

    Article  PubMed  Google Scholar 

  • Zhang L, Yuan D, Yu S, Li Z, Cao Y, Miao Z, Qian H, Tang K (2004) Preference of simple sequence repeats in coding and non-coding regions of Arabidopsis thaliana. Bioinformatics 20:1081–1086

    Article  PubMed  CAS  Google Scholar 

  • Zhao J, Neher DA, Fu S, Li Z, Wang K (2013) Non target effects of herbicides on soil nematode assemblages. Pest Manag Sci 69:679–684

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Ken Drees for running the fragments on the genetic analyzer. We also thank Michael Michelson for help with field collections and necropsies. We thank the University of North Dakota for use of their facilities. This work was done in partial completion of a M.S. Biology degree for Kyle Gustafson at the University of North Dakota.

Funding

The project was funded by a University of North Dakota Faculty Seed Grant and USDA Forest Service Agreement No. 09-CS-11011801-005.

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Authors and Affiliations

  1. Department of Biology, University of North Dakota, Grand Forks, ND, 58208, USA

    Kyle D. Gustafson, Robert A. Newman, Turk Rhen & Vasyl V. Tkach

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  1. Kyle D. Gustafson
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  2. Robert A. Newman
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  3. Turk Rhen
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  4. Vasyl V. Tkach
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Contributions

All authors designed the study. KG collected data. All authors contributed to microsatellite panel development. KG and RN analyzed the data. All authors contributed to writing the manuscript and approved the final version.

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Correspondence to Kyle D. Gustafson.

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Gustafson, K.D., Newman, R.A., Rhen, T. et al. Spatial and genetic structure of directly-transmitted parasites reflects the distribution of their specific amphibian hosts. Popul Ecol 60, 261–273 (2018). https://doi.org/10.1007/s10144-018-0605-x

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