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Phylogenetic heritability of geographic range size in haematophagous ectoparasites: time of divergence and variation among continents

Published online by Cambridge University Press:  12 April 2018

Boris R. Krasnov Open the ORCID record for Boris R. Krasnov [Opens in a new window] ,
Georgy I. Shenbrot ,
Luther van der Mescht ,
Elizabeth M. Warburton  and
Irina S. Khokhlova
Boris R. Krasnov*
Affiliation:
Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben-Gurion 8499000, Israel
Georgy I. Shenbrot
Affiliation:
Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben-Gurion 8499000, Israel
Luther van der Mescht
Affiliation:
Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben-Gurion 8499000, Israel Wyler Department of Dryland Agriculture, French Associates Institute for Agriculture and Biotechnology of Drylands, Jacob Blaustein Institutes for Desert Research, Ben-Gurion, University of the Negev, Midreshet Ben-Gurion 84990, Israel
Elizabeth M. Warburton
Affiliation:
Mitrani Department of Desert Ecology, Swiss Institute for Dryland Environmental and Energy Research, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben-Gurion 8499000, Israel
Irina S. Khokhlova
Affiliation:
Wyler Department of Dryland Agriculture, French Associates Institute for Agriculture and Biotechnology of Drylands, Jacob Blaustein Institutes for Desert Research, Ben-Gurion, University of the Negev, Midreshet Ben-Gurion 84990, Israel
*
Author for correspondence: Boris R. Krasnov, E-mail: krasnov@bgu.ac.il
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Abstract

To understand existence, patterns and mechanisms behind phylogenetic heritability in the geographic range size (GRS) of parasites, we measured phylogenetic signal (PS) in the sizes of both regional (within a region) and continental (within a continent) geographic ranges of fleas in five regions. We asked whether (a) GRS is phylogenetically heritable and (b) the manifestation of PS varies between regions. We also asked whether geographic variation in PS reflects the effects of the environment's spatiotemporal stability (e.g. glaciation disrupting geographic ranges) or is associated with time since divergence (accumulation differences among species over time). Support for the former hypothesis would be indicated by stronger PS in southern than in northern regions, whereas support for the latter hypothesis would be shown by stronger PS in regions with a large proportion of species belonging to the derived lineages than in regions with a large proportion of species belonging to the basal lineages. We detected significant PS in both regional and continental GRSs of fleas from Canada and in continental GRS of fleas from Mongolia. No PS was found in the GRS of fleas from Australia and Southern Africa. Venezuelan fleas demonstrated significant PS in regional GRS only. Local Indicators of Phylogenetic Association detected significant local positive autocorrelations of GRS in some clades even in regions in which PS has not been detected across the entire phylogeny. This was mainly characteristic of younger taxa.

Keywords

Fleasgeographic range sizeLocal Indicators of Phylogenetic Associationphylogeny
Type
Research Article
Information
Parasitology , Volume 145 , Issue 12 , October 2018 , pp. 1623 - 1632
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Copyright
Copyright © Cambridge University Press 2018 

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References

Abellán, P and Ribera, I (2011) Geographic location and phylogeny are the main determinants of the size of the geographical range in aquatic beetles. BMC Evolutionary Biology 11, 344.Google Scholar
Alhajeri, BH, Hunt, OJ and Steppan, SJ (2015) Molecular systematics of gerbils and deomyines (Rodentia: Gerbillinae, Deomyinae) and a test of desert adaptation in the tympanic bulla. Journal of Zoological Systematics and Evolutionary Research 53, 312–330.Google Scholar
Andersen, BG and 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. Oslo, Norway: Scandinavian University Press.Google Scholar
Anselin, L (1995) Local indicators of spatial association – LISA. Geographical Analysis 27, 93–115.Google Scholar
Barraclough, TG, Vogler, AP and Harvey, PH (1998) Revealing the factors that promote speciation. Philosophical Transactions of the Royal Society of London B 353, 241–249.Google Scholar
Blomberg, SP, Garland, T Jr. and Ives, AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57, 717–745.Google Scholar
Brown, JH (1984) On the relationship between abundance and distribution of species. American Naturalist 124, 255–279.Google Scholar
Brown, JH, Stevens, GC and Kaufman, DM (1996) The geographic range: size, shape, boundaries, and internal structure. Annual Review of Ecology and Systematics 27, 597–623.Google Scholar
Cardillo, M (2015) Geographic range shifts do not erase the historic signal of speciation in mammals. American Naturalist 185, 343–353.Google Scholar
Carotenuto, F, Barbera, C and Raia, P (2010) Occupancy, range size, and phylogeny in Eurasian Pliocene to recent large mammals. Paleobiology 36, 399–414.Google Scholar
Eeley, HAC and Foley, RA (1999) Species richness, species range size and ecological specialization among African primates: geographical patterns and conservation implications. Biodiversity and Conservation 8, 1033–1056.Google Scholar
Freckleton, RP, Harvey, PH and Pagel, M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. American Naturalist 160, 712–726.Google Scholar
Gaston, KJ (2003) The Structure and Dynamics of Geographic Ranges. NY: Oxford University Press.Google Scholar
Gaston, KJ (2008) Biodiversity and extinction: the dynamics of geographic range size. Progress in Physical Geography 32, 678–683.Google Scholar
Gaston, KJ and Blackburn, TM (1996) Range size-body size relationships: evidence of scale dependence. Oikos 75, 479–485.Google Scholar
Gittleman, JL and Kot, M (1990) Adaptation: statistics and a null model for estimating phylogenetic effects. Systematic Zoology 39, 227.Google Scholar
Hackathon, R, et al. (2017) Phylobase: Base Package for Phylogenetic Structures and Comparative Data. R package version 0.8.4. https://CRAN.R-project.org/package=phylobase.Google Scholar
Hadfield, JD, et al. (2014) A tale of two phylogenies: comparative analyses of ecological interactions. American Naturalist 183, 174–187.Google Scholar
Herrera-Alsina, L and Villegas-Patraca, R (2014) Biologic interactions determining geographic range size: a one species response to phylogenetic community structure. Ecology and Evolution 4, 968–976.Google Scholar
Holt, RD (2003) On the evolutionary ecology of species’ ranges. Evolutionary Ecology Research 5, 159–178.Google Scholar
Hopkins, GHE and Rothschild, M (1953) An Illustrated Catalogue of the Rothschild Collection of Fleas (Siphonaptera) in the British Museum (Natural History), Vol. I. Tungidae and Pulicidae. London: The Trustees of the British Museum.Google Scholar
Hopkins, GHE and Rothschild, M (1962) An Illustrated Catalogue of the Rothschild Collection of Fleas (Siphonaptera) in the British Museum (Natural History), Vol. III. Hystrichopsyllidae. London: The Trustees of the British Museum.Google Scholar
Hopkins, GHE and Rothschild, M (1966) An Illustrated Catalogue of the Rothschild Collection of Fleas (Siphonaptera) in the British Museum (Natural History), Vol. IV. Hystrichopsyllidae. London: The Trustees of the British Museum.Google Scholar
Hunt, G, Roy, K and Jablonski, D (2005) Species-level heritability reaffirmed: a comment on “On the heritability of geographic range sizes”. American Naturalist 166, 129–135.Google Scholar
Jablonski, D (1987) Heritability at the species level: analysis of geographic ranges of Cretaceous mollusks. Science 238, 360–363.Google Scholar
Jansson, R and Dynesius, M (2002) The fate of clades in a world of recurrent climatic change: Milankovitch oscillations and evolution. Annual Review of Ecology and Systematics 33, 741–777.Google Scholar
Keck, F (2015) Phylosignal: Exploring the Phylogenetic Signal in Continuous Traits. R package version 1.1. https://CRAN.R-project.org/package=phylosignal.Google Scholar
Keck, F, et al. (2016) Phylosignal: an R package to measure, test, and explore the phylogenetic signal. Ecology and Evolution 6, 2774–2780.Google Scholar
Krasnov, BR (2008) Functional and Evolutionary Ecology of Fleas. A Model for Ecological Parasitology. Cambridge, UK: Cambridge University Press.Google Scholar
Krasnov, BR and Shenbrot, GI (2002) Coevolutionary events in history of association of jerboas (Rodentia: Dipodidae) and their flea parasites. Israel Journal of Zoology 48, 331–350.Google Scholar
Krasnov, BR, et al. (2001) The effect of temperature and humidity on the survival of pre-imaginal stages of two flea species (Siphonaptera: Pulicidae). Journal of Medical Entomology 38, 629–637.Google Scholar
Krasnov, BR, et al. (2005a) Host specificity and geographic range in haematophagous ectoparasites. Oikos 108, 449–456.Google Scholar
Krasnov, BR, et al. (2005b) Diversification of ectoparasite assemblages and climate: an example with fleas parasitic on small mammals. Global Ecology and Biogeography 14, 167–175.Google Scholar
Krasnov, BR, Poulin, R and Mouillot, D (2011) Scale-dependence of phylogenetic signal in ecological traits of ectoparasites. Ecography 34, 114–122.Google Scholar
Krasnov, BR, et al. (2015) Assembly rules of ectoparasite communities across scales: combining patterns of abiotic factors, host composition, geographic space, phylogeny and traits. Ecography 38, 184–197.Google Scholar
Lin, G, et al. (2014) Comparative phylogeography of the plateau zokor (Eospalax baileyi) and its host-associated flea (Neopsylla paranoma) in the Qinghai–Tibet Plateau. BMC Evolutionary Biology 14, 180.Google Scholar
Lockwood, JL, et al. (2002) A metric for analyzing taxonomic patterns of extinction risk. Conservation Biology 16, 1137–1142.Google Scholar
Losos, JB (2008) Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecology Letters 11, 995–1007.Google Scholar
Lu, L and Wu, H (2005) Morphological phylogeny of Geusibia Jordan, 1932 (Siphonaptera: Leptopsyllidae) and the host-parasite relationships with pikas. Systematic Parasitology 61, 65–78.Google Scholar
Maddison, WP and Maddison, DR (2017) Mesquite: A Modular System for Evolutionary Analysis. Version 3.31. http://mesquiteproject.org.Google Scholar
McCoy, KD (2003) Sympatric speciation in parasites: what is sympatry? Trends in Parasitology 19, 400–404.Google Scholar
Medvedev, SG (1998) Classification of fleas (order Siphonaptera) and its theoretical foundations. Entomological Review 78, 1080–1093.Google Scholar
Medvedev, SG (2005) An Attempted System Analysis of the Evolution of the Order of Fleas (Siphonaptera). Lectures in Memoriam N. A. Kholodkovsky, No. 57. Saint Petersburg, Russia: Russian Entomological Society and Zoological Institute of Russian Academy of Sciences (in Russian).Google Scholar
Moran, PAP (1948) The interpretation of statistical maps. Journal of the Royal Statistical Society B 10, 243–251.Google Scholar
Moran, PAP (1950) Notes on continuous stochastic phenomena. Biometrika 37, 17–23.Google Scholar
Mouillot, D and Gaston, KJ (2007) Geographical range size heritability: what do neutral models with different modes of speciation predict? Global Ecology and Biogeography 16, 367–380.Google Scholar
Mouillot, D and Gaston, KJ (2009) Spatial overlap enhances geographic range size conservatism. Ecography 32, 671–675.Google Scholar
Mouillot, D, et al. (2006) Conservatism of host specificity in parasites. Ecography 29, 596–602.Google Scholar
Münkemüller, T, et al. (2012) How to measure and test phylogenetic signal. Methods in Ecology and Evolution 3, 743–756.Google Scholar
Nuismer, SL and Kirkpatrick, M (2003) Gene flow and the coevolution of parasite range. Evolution 57, 746–754.Google Scholar
Pagel, M (1999) Inferring the historical patterns of biological evolution. Nature 401, 877–884.Google Scholar
Pavoine, S, et al. (2008) Testing for phylogenetic signal in phenotypic traits: new matrices of phylogenetic proximities. Theoretical Population Biology 73, 79–91.Google Scholar
Peterson, AT, Soberón, J and Sánchez-Cordero, V (1999) Conservatism of ecological niches in evolutionary time. Science 285, 1265–1267.Google Scholar
Pigot, AL, Owens, IPF and Orme, CDL (2010) The environmental limits to geographic range expansion in birds. Ecology Letters 13, 705–715.Google Scholar
Poulin, R, et al. (2006) Evolution of host specificity in fleas: is it directional and irreversible? International Journal for Parasitology 36, 185–191.Google Scholar
Poulin, R, et al. (2011) The comparative ecology and biogeography of parasites. Philosophical Transactions of the Royal Society of London B 366, 2379–2390.Google Scholar
R Development Core Team (2017) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/.Google Scholar
Shenbrot, GI, Krasnov, BR and Lu, L (2007) Geographical range size and host specificity in ectoparasites: a case study with Amphipsylla fleas and rodent hosts. Journal of Biogeography 34, 1679–1690.Google Scholar
Slatyer, RA, Hirst, M and Sexton, JP (2013) Niche breadth predicts geographical range size: a general ecological pattern. Ecology Letters 16, 1104–1114.Google Scholar
Théron, A and Combes, C (1995) Asynchrony of infection timing, habitat preference, and sympatric speciation of schistosome parasites. Evolution 49, 372–375.Google Scholar
Tipton, VJ and Machado-Allison, CE (1972) Fleas of Venezuela. Bringham Young University Science Bulletin. Biological Series 17, 1–115.Google Scholar
Traub, R (1980) The zoogeography and evolution of some fleas, lice and mammals. In Traub, R and Starke, H (eds). Fleas. Proceedings of the International Conference on Fleas, Ashton Wold, Peterborough, UK, 21–25 June 1977. Rotterdam, The Netherlands: A.A. Balkema, pp. 93–172.Google Scholar
van der Mescht, L, Matthee, S and Matthee, CA (2015) A genetic perspective on the taxonomy and evolution of the medically important flea, Dinopsyllus ellobius (Siphonaptera: Dinopsyllinae), and the resurrection of Dinopsyllus abaris. Biological Journal of the Linnean Society 116, 541–557.Google Scholar
Webb, TJ and Gaston, KJ (2003) On the heritability of geographic range sizes. American Naturalist 161, 553–566.Google Scholar
Whiting, MF, et al. (2008) A molecular phylogeny of fleas (Insecta: Siphonaptera): origins and host associations. Cladistics 24, 677–707.Google Scholar
Zacaï, A, et al. (2017) Phylogenetic conservatism of species range size is the combined outcome of phylogeny and environmental stability. Journal of Biogeography 44, 2451–2462.Google Scholar
Zhu, Q, et al. (2015) Fleas (Siphonaptera) are Cretaceous, and evolved with Theria. Molecular Phylogenetics and Evolution 90, 129–139.Google Scholar