Skip to main content
SpringerLink
Log in

Historical biogeography of fleas: the former Bering Land Bridge and phylogenetic dissimilarity between the Nearctic and Palearctic assemblages

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

We investigated the phylogenetic structure of flea assemblages collected from small mammals on opposite sides of and increasing distance from the former Bering Land Bridge (BLB) using crossed double principal coordinate analysis (crossed-DPCoA). Phylogenetic composition of flea assemblages differed substantially between continents, but phylogenetic similarity between the Nearctic and Palearctic assemblages was the highest in the regions closer to the BLB. Within continents, phylogenetic similarity of flea assemblages was lower between regions closer to the BLB and those farther from the BLB than among regions within each of these groups. The Palearctic assemblages were represented mainly by basal families, while the Nearctic assemblages were dominated by a derived family (Ceratophyllidae), suggesting predominantly eastward pre-glaciation movements. In contrast, within the youngest flea family (Ceratophyllidae), the basal clades were characteristic for the Nearctic, while some species of a few derived clades were characteristic for the Palearctic, suggesting that, at least, during glaciation, westward movements occurred as well. In addition, multiple within-family clades of fleas were represented on opposite sides of the BLB suggesting multiple colonization events. This study is the first attempt to apply modern analytical methods of community ecology to reveal patterns in historical biogeography.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Andersen BG, Borns HW Jr (1994) The Ice Age World: an introduction to Quaternary history and research with emphasis on North America and Northern Europe during the last 2.5 million years. Scandinavian University Press, Oslo

    Google Scholar 

  • Arbiv A, Khokhlova IS, Ovadia O, Novoplansky A, Krasnov BR (2012) Use it or lose it: reproductive implications of experimental host shifting in a haematophagousectoparasite. J Evol Biol 25:1140–1147

    Article  CAS  PubMed  Google Scholar 

  • Brooks DR, León-Règagnon V, McLennan DA, Zelmer D (2006) Ecological fitting as a determinant of the community structure of platyhelminth parasites of anurans. Ecology 87:S76–S85

    Article  PubMed  Google Scholar 

  • Chessel D, Dufour AB, Thioulouse J (2004) The ade4 package-I: one-table methods. R News 4:5–10

    Google Scholar 

  • Conroy CJ, Cook JA (2000) Molecular systematics of a Holarctic rodent (Microtus: Muridae). J Mammal 81:344–359

    Article  Google Scholar 

  • Cook JA, Runck A, Conroy CJ (2004) Historical biogeography at the crossroads of the northern continents: molecular phylogenetics of red-backed voles (Rodentia: Arvicolinae). Mol Phylogenet Evol 30:767–777

    Article  CAS  PubMed  Google Scholar 

  • Demboski JR, Cook JA (2003) Phylogenetic diversification within the Sorexcinereus group (Insectivora: Soricidae). J Mammal 84:144–158

    Article  Google Scholar 

  • R Development Core Team (2013) R: a language and environment for statistical computing. - R Foundation for Statistical Computing. Vienna. http://www.R-project.org

  • Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20

    Google Scholar 

  • Dray S, Dufour AB, Chessel D (2007) The ade4 package-II: two-table and K-table methods. R News 7:47–52

    Google Scholar 

  • Eddingsaas AA, Jacobsen BK, Lessa EP, Cook JA (2004) Evolutionary history of the arctic ground squirrel (Spermophilusparryii) in Nearctic Beringia. J Mammal 85:601–610

    Article  Google Scholar 

  • Elias SA, Short SK, Nelson CH, Birks HH (1996) Life and times of the Bering land bridge. Nature 382:60–63

    Article  CAS  Google Scholar 

  • Galbreath KE, Cook JA (2004) Genetic consequences of Pleistocene glaciations for the tundra vole (Microtusoeconomus) in Beringia. Mol Ecol 13:135–148

    Article  CAS  PubMed  Google Scholar 

  • Galbreath KE, Hoberg EP (2012) Return to Beringia: parasites reveal cryptic biogeographic history of North American pikas. Proc Roy Soc Lond B 279:371–378

    Article  Google Scholar 

  • Galbreath KE, Cook JA, Eddingsaas AA, Dechaine EG (2011) Diversity and demography in Beringia: multilocus tests of paleodistribution models reveal the complex history of arctic ground squirrels. Evolution 65:1879–1896

    Article  PubMed  Google Scholar 

  • Galbreath KE, Ragaliauskaite K, Kontrimavichus L, Makarikov AA, Hoberg EP (2013) A widespread distribution for Arostrilepistenuicirrosa (Eucestoda: Hymenolepididae) in Myodes voles (Cricetidae: Arvicolinae) from the Palearctic based on molecular and morphological evidence: historical and biogeographic implications. Acta Parasitol 58:441–452

    Article  PubMed  Google Scholar 

  • Gotelli NJ, McCabe DJ (2002) Species co-occurrence: a meta-analysis of J. M. Diamond’s assembly rules model. Ecology 83:2091–2096

    Article  Google Scholar 

  • Gotelli NJ, Rohde K (2002) Co-occurrence of ectoparasites of marine fishes: a null model analysis. Ecol Lett 5:86–94

    Article  Google Scholar 

  • Harbison CW, Clayton DH (2011) Community interactions govern host-switching with implications for host-parasite coevolutionary history. Proc Natl Acad Sci USA 108:9525–9529

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Harrison RG, Bogdanowicz SM, Hoffmann RS, Yensen E, Sherman PW (2003) Phylogeny and evolutionary history of the ground squirrels (Rodentia: Marmotinae). J Mamm Evol 10:249–276

    Article  Google Scholar 

  • Haukisalmi V, Henttonen H, Hardman LM (2006) Taxonomy and diversity of Paranoplocephala spp. (Cestoda: Anoplocephalidae) in voles and lemmings of Beringia, with a description of three new species. Biol J Linn Soc 89:277–279

    Article  Google Scholar 

  • Hoberg EP (2005) Coevolution and biogeography among Nematodirinae (Nematoda: Trichostrongylina) Lagomorpha and Artiodactyla (Mammalia): exploring determinants of history and structure for the northern fauna across the Holarctic. J Parasitol 91:358–369

    Article  PubMed  Google Scholar 

  • Hoberg EP, Monsen KJ, Kutz S, Blouin MS (1999) Structure, biodiversity, and historical biogeography of nematode faunas in Holarctic ruminants: morphological and molecular diagnoses for Teladorsagiaboreoarcticus n. sp. (Nematoda: Ostertagiinae), a dimorphic cryptic species in muskoxen, Ovibosmoschatus. J Parasitol 85:910–934

    Article  CAS  PubMed  Google Scholar 

  • Hoberg EP, Galbreath KE, Cook JA (2003) Arctic biodiversity: from discovery to faunal baselines – revealing the history of a dynamic ecosystem. J Parasitol 89:584–595

    Google Scholar 

  • Hoberg EP, Galbreath KE, Cook JA, Kutz SJ, Pottey L (2012) Northern host-parasite assemblages: history and biogeography on the borderlands of episodic climate and environmental transition. Adv Parasitol 79:1–97

    Article  PubMed  Google Scholar 

  • Hope AG, Takebayashi N, Galbreath KE, Talbot SL, Cook JA (2013) Temporal, spatial and ecological dynamics of speciation among amphi-Beringian small mammals. J Biogeogr 40:415–429

    Article  Google Scholar 

  • Hopkins DM (1959) Cenozoic history of the Bering Land Bridge. Science 129:1519–1528

    Article  CAS  PubMed  Google Scholar 

  • Hopkins DM (1967) The Bering Land Brige. Stanford University Press, Stanford

    Google Scholar 

  • Hopkins DM, Matthews JV Jr, Schweder CE, Young SB (eds) (1982) Paleoecology of Beringia. Academic Press, New York

    Google Scholar 

  • Hulten E (1937) Outline of the history of Arctic and boreal biota during the Quaternary period. Lehre J. Cramer, New York

    Google Scholar 

  • Janzen DH (1985) On ecological fitting. Oikos 45:308–310

    Article  Google Scholar 

  • Khokhlova IS, Fielden LJ, Degen AA, Krasnov BR (2012) Ectoparasite fitness in auxiliary hosts: phylogenetic distance from a principal host matters. J Evol Biol 25:2005–2013

    Article  CAS  PubMed  Google Scholar 

  • Khokhlova IS, Pilosof S, Fielden LJ, Krasnov BR, Degen AA (2014) A trade-off between quantity and quality of offspring in haematophagousectoparasites: the effect of the level of specialization. J Anim Ecol 83:397–405

    Article  Google Scholar 

  • Korine C, Krasnov BR, Khokhlova IS, Pinshow B (2012) Effects of host diet and thermal state on feeding performance of the flea Xenopsyllaramesis. J Exp Biol 215:1435–1441

    Article  PubMed  Google Scholar 

  • Krasnov BR (2008) Functional and evolutionary ecology of fleas. A model for ecological parasitology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Krasnov BR, Shenbrot GI (2003) Coevolutionary events in history of association of jerboas (Rodentia: Dipodidae) and their flea parasites. Isr J Zool 48:331–350

    Article  Google Scholar 

  • Krasnov BR, Khokhlova IS, Fielden LJ, Burdelova NV (2001) The effect of air temperature and humidity on the survival of pre-imaginal stages of two flea species (Siphonaptera: Pulicidae). J Med Entomol 38:629–637

    Article  CAS  PubMed  Google Scholar 

  • Krasnov BR, Poulin R, Shenbrot GI, Mouillot D, Khokhlova IS (2004) Ectoparasitic “jacks-of-all-trades”: relationship between abundance and host specificity in fleas (Siphonaptera) parasitic on small mammals. Am Nat 164:506–515

    Article  PubMed  Google Scholar 

  • Krasnov BR, Shenbrot GI, Khokhlova IS, Poulin R (2006) Is abundance a species attribute of haematophagousectoparasites? Oecologia 150:132–140

    Article  PubMed  Google Scholar 

  • Krasnov BR, Korine C, Burdelova NV, Khokhlova IS, Pinshow B (2007) Between-host phylogenetic distance and feeding efficiency in haematophagousectoparasites: rodent fleas and a bat host. Parasitol Res 101:365–371

    Article  PubMed  Google Scholar 

  • Krasnov BR, Poulin R, Mouillot D (2011) Scale-dependence of phylogenetic signal in ecological traits of ectoparasites. Ecography 34:114–122

    Article  Google Scholar 

  • Kurten B (1971) The age of mammals. Weidenfeld and Nicolson, London

    Google Scholar 

  • Lu L, Wu H (2005) Morphological phylogeny of Geusibia Jordan, 1932 (Siphonaptera: Leptopsyllidae) and the host-parasite relationships with pikas. Syst Parasitol 61:65–78

    Article  Google Scholar 

  • McKenna MC (1972) Was Europe connected directly to North America prior to the middle Eocene. In: Dobzhansky T, Hecht MK, Steere WC (eds) Evolutionary biology 6. Appleton-Century-Crofts, New York, pp 179–189

    Chapter  Google Scholar 

  • Medvedev SG (1996) Geographical distribution of families of fleas (Siphonaptera). Entomol Rev 76:978–992

    Google Scholar 

  • Medvedev SG (1998) Fauna and host-parasite relations of fleas (Siphonaptera) in the Palaearctic. Entomol Rev 78:292–308

    Google Scholar 

  • Medvedev SG (2000a) Fauna and host-parasite associations of fleas (Siphonaptera) in different zoogeographical regions of the World. I. Entomol Rev 80:409–435

    Google Scholar 

  • Medvedev SG (2000b) Fauna and host-parasite associations of fleas (Siphonaptera) in different zoogeographical regions of the World. II. Entomol Rev 80:640–655

    Google Scholar 

  • Medvedev SG (2014) The Palaearctic centers of taxonomic diversity of fleas. (Siphonaptera). Entomol Rev 94:345–358

    Article  Google Scholar 

  • Nieberding CM, Olivieri I (2007) Parasites: proxies for host genealogy and ecology. Trends Ecol Evol 22:156–165

    Article  PubMed  Google Scholar 

  • Pavoine S, Dufour AB, Chessel D (2004) From dissimilarities among species to dissimilarities among communities: a double principal coordinate analysis. J Theor Biol 228:523–537

    Article  PubMed  Google Scholar 

  • Pavoine S, Blondel J, Dufour AB, Gasc A, Bonsall MB (2013) A new technique for analysing interacting factors affecting bodiversitypatterns: crossed-DPCoA. PLoS ONE 8:e54530

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Peus F (1968) Über die beiden Bernstein-Flöhe (Insecta, Siphonaptera). Palaeontologische Zeitschrift 42:62–72

    Article  Google Scholar 

  • Pielou EC (1991) After the Ice Age. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Poulin R (2007) Evolutionary ecology of parasites: from individuals to communities, 2nd edn. Princeton University Press, Princeton

    Google Scholar 

  • Rao CR (1982) Diversity and dissimilarity coefficients: a unified approach. Theor Pop Biol 21:24–43

    Article  Google Scholar 

  • Rao CR (1984) Convexity properties of entropy functions and analysis of diversity. Inequalities Stat Probab 5:68–77

    Article  Google Scholar 

  • Rao CR (1986) Rao’s axiomatization of diversity measures. In: Kotz S, Johnson NL (eds) Encyclopedia of statistical sciences. Wiley, New York, pp 614–617

    Google Scholar 

  • Rausch R (1994) Transberingian dispersal of cestodes in mammals. Int J Parasitol 24:1203–1212

    Article  CAS  PubMed  Google Scholar 

  • Scotese CR, Golonka J (1992) PALEOMAP Paleogeographic Atlas, PALEOMAP Progress Report No. 20-0692. Department of Geology, University of Texas at Arlington, Arlington

    Google Scholar 

  • Sher A (1999) Traffic lights at the Beringian crossroads. Nature 397:103–104

    Article  CAS  Google Scholar 

  • Simpson GG (1950) History of the fauna of Latin America. Am Sci 38:361–389

    Google Scholar 

  • Stehli FG, Webb SD (eds) (1985) The great American interchange. Plenum Press, New York

    Google Scholar 

  • Swanson DK (2003) A comparison of taiga flora in north-eastern Russia and Alaska/Yukon. J Biogeogr 30:1109–1121

    Article  Google Scholar 

  • Traub R (1980) The zoogeography and evolution of some fleas, lice and mammals. In: Traub R, Starke H (eds) Fleas. Proceedings of the International Conference on Fleas, Ashton Wold, Peterborough, UK, 21-25 June 1977. A.A. Balkema, Rotterdam, pp 93-172

  • Traub R (1985) Coevolution of fleas and mammals. In: Kim KC (ed) Coevolution of parasitic arthropods and mammals. Wiley, New York, pp 295–437

    Google Scholar 

  • Vuilleumier BS (1971) Pleistocene changes in the fauna and flora of South America. Science 173:771–780

    Article  CAS  PubMed  Google Scholar 

  • Waltari E, Hoberg EP, Lessa EP, Cook JA (2007) Eastward Ho: phylogeographical perspectives on colonization of hosts and parasites across the Beringian nexus. J Biogeogr 34:561–574

    Article  Google Scholar 

  • Whiting MF, Whiting AS, Hastriter MW, Dittmar K (2008) A molecular phylogeny of fleas (Insecta: Siphonaptera): origins and host associations. Cladistics 24:677–707

    Article  Google Scholar 

  • Wickström L, Haukisalmi V, Varis S, Hantula J, Fedorov VB, Henttonen H (2003) Phylogeography of circumpolar Paranoplocephalaarctica species complex (Cestoda: Anoplocephalidae) parasitizing collared lemmings. Mol Ecol 12:3359–3371

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Allan Degen for helpful comments on the earlier version of the manuscript. This study was partly supported by grant from the Israel Science Foundation (grant No. 26/12 to B.R.K. and I.S.K.). This is publication no. 858 of the Mitrani Department of Desert Ecology.

Author information

Authors and Affiliations

  1. Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institute for Desert Research, Ben-Gurion University, Negev, SedeBoqer Campus, 84990, Midreshet Ben-Gurion, Israel

    Boris R. Krasnov & Georgy I. Shenbrot

  2. Wyler Department of Dryland Agriculture, French Associates Institute for Agriculture and Biotechnology of Drylands, Jacob Blaustein Institute for Desert Research, Ben-Gurion University, Negev, SedeBoqer Campus, 84990, Midreshet Ben-Gurion, Israel

    Irina S. Khokhlova

Authors
  1. Boris R. Krasnov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Georgy I. Shenbrot
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Irina S. Khokhlova
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Boris R. Krasnov.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online Resource 1

(DOCX 24 kb)

Online Resource 2

(DOCX 489 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Krasnov, B.R., Shenbrot, G.I. & Khokhlova, I.S. Historical biogeography of fleas: the former Bering Land Bridge and phylogenetic dissimilarity between the Nearctic and Palearctic assemblages. Parasitol Res 114, 1677–1686 (2015). https://doi.org/10.1007/s00436-015-4349-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-015-4349-7

Keywords

Search

Navigation