Skip to main content
SpringerLink
Log in

Distribution, prevalence and host specificity of avian malaria parasites across the breeding range of the migratory lark sparrow (Chondestes grammacus)

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

The lark sparrow (Chondestes grammacus) is a ground-nesting passerine that breeds across much of the central North American steppe and sand barrens. Through genotyping and sequencing of avian malaria parasites we examined levels of malaria prevalence and determined the distribution of Haemoproteus and Plasmodium lineages across the breeding range of the lark sparrow. Analysis of 365 birds collected from five breeding locations revealed relatively high levels of malaria prevalence in adults (80 %) and juveniles (46 %), with infections being primarily of Haemoproteus (91 % of sequenced samples). Levels of genetic diversity and genetic structure of malaria parasites with respect to the avian host populations revealed distinct patterns for Haemoproteus and Plasmodium, most likely as a result of their distinct life histories, host specificity, and transmission vectors. With the exception of one common Haemoproteus haplotype detected in all populations, all other haplotypes were either population-specific or shared by two to three populations. A hierarchical analysis of molecular variance of Haemoproteus sequences revealed that 15–18 % of the genetic variation can be explained by differences among host populations/locations (p < 0.001). In contrast to the regional patterns of genetic differentiation detected for the lark sparrow populations, Haemoproteus parasites showed high levels of population-specific variation and no significant differences among regions, which suggests that the population dynamics of the parasites may be driven by evolutionary processes operating at small spatial scales (e.g., at the level of host populations). These results highlight the potential effects of host population structure on the demographic and evolutionary dynamics of parasites.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Atkinson CT, Van Riper C III (1991) Pathogenicity and epizootiology of avian hematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. In: Loye JL, Zuk M (eds) Bird–parasite interactions. Ecology, evolution, and behavior. Oxford University Press, New York, pp 20–48

    Google Scholar 

  • Atkinson CT, Woods KL, Dusek RJ, Sileo LS, Iko WM (1995) Wildlife diseases and conservation in Hawaii: pathogenicity of avian malaria (Plasmodium relictum) in experimentally infected Iiwi (Vestiaria coccinea). Parasitology 111:S59–S69

    Article  PubMed  Google Scholar 

  • Atkinson CT, Dusek RJ, Woods KL, Iko WM (2000) Pathogenicity of avian malaria in experimentally-infected Hawaii Amakihi. J Wildl Dis 36:197–204

    Article  CAS  PubMed  Google Scholar 

  • Baepler DH (1968) Chondestes grammacus: Lark Sparrow. In: Bent AC (ed) Life histories of North American cardinals, grosbeaks, buntings, towhees, finches, sparrows, and allies. U.S. National Museum Bulletin 237. Smithsonian Institution Press, Washington D.C., pp 886–902

  • Beadell JS, Fleischer RC (2005) A restriction enzyme-based assay to distinguish between avian Hemosporidians. J Parasit 91:683–685

    Article  CAS  PubMed  Google Scholar 

  • Beadell JS, Gering E, Austin J, Dumbacher JP, Peirce MA, Pratt TK, Atkinson CT, Fleischer RC (2004) Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Mol Ecol 13:3829–3844

    Article  PubMed  Google Scholar 

  • Beadell JS, Ishtiaq F, Covas R, Melo M, Warren BH, Atkinson CT, Bensch S, Graves GR, Jhala YV, Peirce MA, Rahmani AR, Fonseca DM, Fleischer RC (2006) Global phylogeographic limits of Hawaii’s avian malaria. Proc R Soc Lond Ser B 273:2935–2944

    Article  Google Scholar 

  • Bensch S, Stjernman M, Hasselquist D, Ostman O, Hansson B, Westerdahl H, Pinheiro RT (2000) Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proc R Soc Lond Ser B 267:1583–1589

    Article  CAS  Google Scholar 

  • Bensch S, Waldenstrom J, Jonzen N, Westerdahl H, Hansson B, Sejberg D, Hasselquist D (2007) Temporal dynamics and diversity of avian malaria parasites in a single host species. J Anim Ecol 76:112–122

    Article  PubMed  Google Scholar 

  • Bonneaud C, Pérez-Tris J, Federici P, Chastel O, Sorci G (2006) Major histocompatibility alleles associated with local resistance to malaria in a passerine. Evolution 60:383–389

    Article  CAS  PubMed  Google Scholar 

  • Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  CAS  PubMed  Google Scholar 

  • Cosgrove CL, Wood MJ, Day KP, Sheldon BC (2008) Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. J Anim Ecol 77:540–548

    Article  PubMed  Google Scholar 

  • Dale S, Kruszewicz A, Slagsvold T (1996) Effects of blood parasites on sexual and natural selection in the pied flycatcher. J Zool 238:373–393

    Article  Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    Article  PubMed Central  PubMed  Google Scholar 

  • Durrant KL, Marra PP, Fallon SM, Colbeck GJ, Gibbs HL, Hobson KA, Norris DR, Bernik B, Lloyd VL, Fleischer RC (2008) Parasite assemblages distinguish populations of a migratory passerine on its breeding grounds. J Zool 274:318–326

    Article  Google Scholar 

  • Escalante AA, Freeland DE, Collins WE, Lal AA (1998) The evolution of primate malaria parasites based on the gene encoding cytochrome b from the linear mitochondrial genome. Proc Natl Acad Sci USA 95:8124–8129

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  PubMed Central  Google Scholar 

  • Fallon SM, Bermingham E, Ricklefs RE (2003) Island and taxon effects in parasitism revisited: avian malaria in the Lesser Antilles. Evolution 57:606–615

    Article  PubMed  Google Scholar 

  • Fallon SM, Bermingham E, Ricklefs RE (2005) Host specialization and geographic localization of avian malaria parasites: a regional analysis in the Lesser Antilles. Am Nat 165:466–480

    Article  PubMed  Google Scholar 

  • Fallon SM, Fleischer RC, Graves GR (2006) Malarial parasites as geographical markers in migratory birds? Biol Lett 2:213–216

    Article  PubMed Central  PubMed  Google Scholar 

  • Felsenstein J (2004) Inferring phylogenies. Sinauer Associates Inc, Sunderland

    Google Scholar 

  • Gibb CE, Jones J, Girvan MK, Barg JJ, Robertson RJ (2005) Geographic variation in prevalence and parasitemia of Haemoproteus paruli in the cerulean warbler (Dendroica cerulea). Can J Zool 83:626–629

    Article  Google Scholar 

  • Griffiths R, Double M, Orr K, Dawson R (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075

    Article  CAS  PubMed  Google Scholar 

  • Hellgren O, Pérez-Tris J, Bensch S (2009) A jack-of-all-trades and still a master of some: prevalence and host range in avian malaria and related blood parasites. Ecology 90:2840–2849

    Article  PubMed  Google Scholar 

  • Ishak HD, Dumbacher JP, Anderson NL, Keane JJ, Valkiūnas G, Haig SM, Tell LA, Sehgal RNM (2008) Blood parasites in owls with conservation implications for the spotted owl (Strix occidentalis). PLoS ONE 3:e2304

    Article  PubMed Central  PubMed  Google Scholar 

  • Kilpatrick AM, LaPointe DA, Atkinson CT, Woodworth BL, Lease JK, Reiter ME, Gross K (2006) Effects of chronic avian malaria (Plasmodium relictum) infection on reproductive success of Hawaii amakihi (Hemignathus virens). Auk 123:764–774

    Article  Google Scholar 

  • Knowles SC, Palinauskas V, Sheldon BC (2010) Chronic malaria infections increase family inequalities and reduce parental fitness: experimental evidence from a wild bird population. J Evol Biol 23:557–569

    Article  CAS  PubMed  Google Scholar 

  • Korpimäki E, Hakkarainen H, Bennett GF (1993) Blood parasites and reproductive success of Tengmalm’s Owl: detrimental effects on females but not on males? Funct Ecol 7:420–426

    Article  Google Scholar 

  • Lachish S, Knowles SCL, Alves R, Wood MJ, Sheldon BC (2011a) Fitness effects of endemic malaria infections in a wild bird population: the importance of ecological structure. J Anim Ecol 80:1196–1206

    Article  PubMed  Google Scholar 

  • Lachish S, Knowles SCL, Alves R, Wood MJ, Sheldon BC (2011b) Infection dynamics of endemic malaria in a wild bird population: parasite species-dependent drivers of spatial and temporal variation in transmission rates. J Anim Ecol 80:1207–1216

    Article  PubMed  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Loiseau C, Harrigan RJ, Robert A, Bowie RCK, Thomassen HA, Smith TB, Sehgal RNM (2012) Host and habitat specialization of avian malaria in Africa. Mol Ecol 21:431–441

    Article  PubMed Central  PubMed  Google Scholar 

  • Longmire JL, Lewis A, Meincke LJ, Hildebrand CE (1986) A new and rapid procedure for the isolation of ultra-high molecular weight eukaryotic DNA. Fed Proc 45:1849

    Google Scholar 

  • Martin JW, Parrish JR (2000) Lark sparrow (Chondestes grammacus). In: Poole A, Gill F (eds) The birds of North America, vol 488. Academy of Natural Sciences, Philadelphia, and American Ornithologists’ Union, Washington

  • Massey JG, Graczyk TK, Cranfield MR (1996) Characteristics of naturally acquired Plasmodium relictum capistranoae infections in naïve Hawaiian crows (Corvus hawaiiensis) in Hawaii. J Parasitol 82:182–185

    Article  CAS  PubMed  Google Scholar 

  • Miller AH (1941) A review of centers of differentiation for birds in the western great basin region. Condor 43:257–267

    Article  Google Scholar 

  • Njabo KY, Cornel AJ, Bonneaud C, Toffelmier E, Sehgal RNM, Valkiūnas G, Russell AF, Smith TB (2011) Nonspecific patterns of vector, host and avian malaria parasite associations in a central African rainforest. Mol Ecol 20:1049–1061

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Oberholser HC (1932) Descriptions of new birds from Oregon, chiefly from the Warner Valley region. Sci Pub Clevel Mus Nat Hist 4:1–12

    Google Scholar 

  • Ortego J, Cordero PJ, Aparicio JM, Calabuig G (2008) Consequences of chronic infections with three different avian malaria lineages on reproductive performance of Lesser Kestrels (Falco naumanni). J Ornithol 149:337–343

    Article  Google Scholar 

  • Outlaw DC, Ricklefs RE (2009) On the phylogenetic relationships of haemosporidian parasites from raptorial birds (Falconiformes and Strigiformes). J Parasitol 95:1171–1176

    Article  CAS  PubMed  Google Scholar 

  • Pagenkopp KM, Klicka J, Durrant KL, Garvin JC, Fleischer RC (2008) Geographic variation in malarial parasite lineages in the common yellowthroat (Geothlypis trichas). Conserv Genet 9:1577–1588

    Article  Google Scholar 

  • Pérez-Tris J, Bensch S, Koella J (2005) Dispersal increases local transmission of avian malarial parasites. Ecol Lett 8:838–845

    Article  Google Scholar 

  • Pérez-Tris J, Hellgren O, Križanauskiene A, Waldenström J, Secondi J, Bonneaud C, Fjeldså J, Hasselquist D, Bensch S (2007) Within-host speciation of malaria parasites. PLoS ONE 2:e235

    Article  PubMed Central  PubMed  Google Scholar 

  • Posada D (2008) jModeltest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  CAS  PubMed  Google Scholar 

  • Ricklefs RE, Fallon SM (2002) Diversification and host switching in avian malaria parasites. Proc R Soc Lond Ser B 269:885–892

    Article  Google Scholar 

  • Ricklefs RE, Outlaw DC (2010) A molecular clock for malaria parasites. Science 329:226–229

    Article  CAS  PubMed  Google Scholar 

  • Ricklefs RE, Fallon SM, Bermingham E (2004) Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. Syst Biol 53:111–119

    Article  PubMed  Google Scholar 

  • Ricklefs RE, Swanson BL, Fallon SM, Martinez-Abrain A, Scheuerlein A, Gray J, Latta SC (2005) Community relationships of avian malaria parasites in southern Missouri. Ecol Monogr 75:543–559

    Article  Google Scholar 

  • Ross JD, Bouzat JL (2014) Genetic and morphometric diversity in the Lark Sparrow (Chondestes grammacus) suggest discontinuous clinal variation across major breeding regions associated with previously characterized subspecies. Auk 131:298–313

    Article  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Sauer JR, Hines JE, Fallon J (2008) The North American breeding bird survey, results and analysis 1966–2007. Version 5.15.2008. USGS Patuxent Wildlife Research Center, Laurel

    Google Scholar 

  • Szöllősi E, Cichoń M, Eens M, Hasselquist D, Kempenaers B, Merino S, Nilsson J-Å, Rosivall B, Rytkönen S, Török J, Wood MJ, Garamszegi LZ (2011) Determinants of distribution and prevalence of avian malaria in blue tit populations across Europe: separating host and parasite effects. J Evol Biol 24:2014–2024

    Article  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Valkiūnas G (2005) Avian malaria parasites and other haemosporidia. CRC Press, Boca Raton

    Google Scholar 

  • van Riper C III, van Riper SG, Goff ML, Laird M (1986) The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecol Monogr 56:327–344

    Article  Google Scholar 

  • Waldenstrom J, Bensch S, Kiboi S, Hasselquist D, Ottosson U (2002) Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Mol Ecol 11:1545–1554

    Article  CAS  PubMed  Google Scholar 

  • Weatherhead PJ (1990) Secondary sexual traits, parasites, and polygyny in red-winged blackbirds, Agelaius pheoniceus. Behav Ecol 1:125–130

    Article  Google Scholar 

  • Wood MJ, Cosgrove CL, Wilkin TA, Knowles SCL, Day KP, Sheldon BC (2007) Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Mol Ecol 16:3263–3273

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Jeremy D. Ross for coordinating collection of blood samples of lark sparrows, V. P. Bingman, M. Herman, T. Herman, E. Keller, J. Noland, and E. A. Ross for field assistance, and Elijah Bodey and Hanna Scheppler for helping in the molecular sexing of birds. We would also like to thank the Editor and three anonymous reviewers for their suggestions on previous versions of the manuscript. We thank the following institutions/individuals for allowing field access to Lark Sparrow populations: Oak Openings Preserve, Metroparks of the Toledo Area; Kitty Todd Nature Preserve, The Nature Conservancy; Lost Mound Unit of Upper Mississippi National Wildlife Refuge, US Fish and Wildlife Service; Cedar Point Biological Station, University of Nebraska at Lincoln; Daniel Brown and Skipper Duncan, Tom Green County, Texas; Hopland Research and Extension Center, University of California at Davis; and Gray Davis/Dye Creek Preserve, The Nature Conservancy; R. C. Dawkins, Angelo State University; D. G. Wenny, Illinois Natural History Survey; and M. C. Shieldcastle, Ohio Department of Natural Resources. This project was funded through State Wildlife Grants from the Ohio Department of Natural Resources Division of Wildlife, in-kind contributions from The Nature Conservancy, and the Department of Biological Sciences at Bowling Green State University.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Bowling Green State University, Bowling Green, OH, 43403, USA

    Bethany L. Swanson, Amanda C. Lyons & Juan L. Bouzat

Authors
  1. Bethany L. Swanson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amanda C. Lyons
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Juan L. Bouzat
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Juan L. Bouzat.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Swanson, B.L., Lyons, A.C. & Bouzat, J.L. Distribution, prevalence and host specificity of avian malaria parasites across the breeding range of the migratory lark sparrow (Chondestes grammacus). Genetica 142, 235–249 (2014). https://doi.org/10.1007/s10709-014-9770-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-014-9770-9

Keywords

Search

Navigation