Hostname: page-component-848d4c4894-4hhp2 Total loading time: 0 Render date: 2024-06-05T10:03:06.345Z Has data issue: false hasContentIssue false
  • English
  • Français

Two lineages of kingfisher feather lice exhibit differing degrees of cospeciation with their hosts

Published online by Cambridge University Press:  03 May 2019

Therese A. Catanach Open the ORCID record for Therese A. Catanach [Opens in a new window] ,
Kevin P. Johnson ,
Ben D. Marks ,
Robert G. Moyle ,
Michel P. Valim  and
Jason D. Weckstein
Therese A. Catanach*
Affiliation:
Department of Ornithology, Academy of Natural Sciences of Drexel University, 1900 Benjamin Franklin Parkway, Philadelphia, PA, 19103, USA
Kevin P. Johnson
Affiliation:
Illinois Natural History Survey, Prairie Research Institute, University of Illinoisat Urbana-Champaign, 1816 S. Oak St., Champaign, IL, 61820, USA
Ben D. Marks
Affiliation:
Field Museum of Natural History, Science and Education, 1400 S. Lake Shore Drive, Chicago, IL 60605, USA
Robert G. Moyle
Affiliation:
Department of Ecology and Evolutionary Biology and Biodiversity Institute, University of Kansas, 1345 Jayhawk Blvd., Lawrence, KS, 66045, USA
Michel P. Valim
Affiliation:
Biotério da Universidade Iguaçu, 2134 Av. Abílio Augusto Távora, Nova Iguaçu, RJ, 26260-045, Brazil
Jason D. Weckstein
Affiliation:
Department of Ornithology, Academy of Natural Sciences of Drexel University, and Department of Biodiversity, Earth, and Environmental Sciences, Drexel University, 1900 Benjamin Franklin Parkway, Philadelphia, PA, 19103, USA
*
Author for correspondence: Therese A. Catanach, E-mail: tacatanach@tamu.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Unlike most bird species, individual kingfisher species (Aves: Alcedinidae) are typically parasitized by only a single genus of louse (Alcedoffula, Alcedoecus, or Emersoniella). These louse genera are typically specific to a particular kingfisher subfamily. Specifically, Alcedoecus and Emersoniella parasitize Halcyoninae, whereas Alcedoffula parasitizes Alcedininae and Cerylinae. Although Emersoniella is geographically restricted to the Indo-Pacific region, Alcedoecus and Alcedoffula are geographically widespread. We used DNA sequences from two genes, the mitochondrial COI and nuclear EF-1α genes, to infer phylogenies for the two geographically widespread genera of kingfisher lice, Alcedoffula and Alcedoecus. These phylogenies included 47 kingfisher lice sampled from 11 of the 19 currently recognized genera of kingfishers. We compared louse phylogenies to host phylogenies to reconstruct their cophylogenetic history. Two distinct clades occur within Alcedoffula, one that infests Alcedininae and a second that infests Cerylinae. All species of Alcedoecus were found only on host species of the subfamily Halcyoninae. Cophylogenetic analysis indicated that Alcedoecus, as well as the clade of Alcedoffula occurring on Alcedininae, do not show evidence of cospeciation. In contrast, the clade of Alcedoffula occurring on Cerylinae showed strong evidence of cospeciation.

Keywords

BiogeographycospeciationlicephylogeneticsPhthiraptera
Type
Research Article
Information
Parasitology , Volume 146 , Issue 8 , July 2019 , pp. 1083 - 1095
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

Current Address: Department of Wildlife and Fisheries Sciences, Texas A&M University College Station, 2258 TAMU, College Station, TX 77843-2258

References

Andersen, MJ, Oliveros, CH, Filardi, CE and Moyle, RG (2013) Phylogeography of the variable dwarf-kingfisher Ceyx lepidus (Aves: Alcedinidae) inferred from mitochondrial and nuclear DNA sequences. The Auk 130, 118–131.Google Scholar
Andersen, MJ, Shult, HT, Cibois, A, Thibault, J-C, Filardi, CE and Moyle, RG (2015) Rapid diversification and secondary sympatry in Australo-Pacific kingfishers (Aves: Alcedinidae: Todiramphus). Royal Society Open Science 2, 140375.Google Scholar
Andersen, MJ, McCullough, JM, Mauck, WM, Smith, BT and Moyle, RG (2017) A phylogeny of kingfishers reveals an Indomalayan origin and elevated rates of diversification on oceanic islands. Journal of Biogeography 45, 269–281.Google Scholar
Banks, JC, Palma, RL and Paterson, AM (2006) Cophylogenetic relationships between penguins and their chewing lice. Journal of Evolutionary Biology 19, 156–166.Google Scholar
Carriker, MA (1959) New species of Mallophaga (Alcedoffula and Philopterus) from Colombia and the United States. Neotropical Miscellany 12, 205–213.Google Scholar
Catanach, TA and Johnson, KP (2015) Independent origins of the feather lice (Insecta: Degeeriella) of raptors. Biological Journal of the Linnaean Society 114, 837–847.Google Scholar
Clay, T and Meinertzhagen, R (1939) New genera and species of Mallophaga. Entomologist 72, 161–168.Google Scholar
Clayton, DH (1990) Host specificity of Strigiphilus owl lice (Ischnocera: Philopteridae), with the description of new species and host associations. Journal of Medical Entomology 27, 257–265.Google Scholar
Clayton, DH and Johnson, KP (2003) Linking coevolutionary history to ecological process: doves and lice. Evolution 57, 2335–2341.Google Scholar
Clayton, DH, Gregory, RD and Price, RD (1992) Comparative ecology of neotropical bird lice. Journal of Animal Ecology 61, 781–795.Google Scholar
Clayton, DH, Bush, SE, Goates, BM and Johnson, KP (2003) Host defense reinforces host-parasite coevolution. Proceedings of the National Academy of Sciences USA 100, 15694–15699.Google Scholar
Clements, JF, Schulenberg, TS, Iliff, MJ, Roberson, D, Fredericks, TA, Sullivan, BL and Wood, CL (2017) The eBird/Clements checklist of birds of the world: v2017. Available at http://www.birds.cornell.edu/clementschecklist/download/.Google Scholar
Conow, C, Fielder, D, Ovadia, Y and Libeskind-Hadas, R (2010) Jane: a new tool for the cophylogeny reconstruction problem. Algorithms for Molecular Biology 5, 16.Google Scholar
Danforth, BN and Ji, S (1998) Elongation factor-1α occurs as two copies in bees: implications for phylogenetic analysis of EF-1α sequences in insects. Molecular Biology and Evolution 15, 225–235.Google Scholar
Drummond, AJ and Rambaut, A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.Google Scholar
Edgar, RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.Google Scholar
Ehrlich, PR and Raven, PH (1964) Butterflies and plants: a study in coevolution. Evolution 18, 586–608.Google Scholar
Gouy, M, Guindon, S and Gascuel, O (2010) Seaview version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27, 221–224.Google Scholar
Groth, JG and Barrowclough, GF (1999) Basal divergences in birds and the phylogenetic utility of the nuclear RAG-1 gene. Molecular Phylogenetics and Evolution 12, 115–123.Google Scholar
Gustafsson, DR and Bush, SE (2014) Three new species of chewing lice of the genus Emersoniella tendeiro, 1965 (Insecta: Phthiraptera: Ischnocera: Philopteridae) from Papua New Guinean kingfishers and kookaburras (Aves: Coraciiformes: Alcedinidae). Zootaxa 3796, 528–544.Google Scholar
Hackett, SJ (1996) Molecular phylogenetics and biogeography of tanagers in the genus Ramphocelus (aves). Molecular Phylogenetics and Evolution 5, 368–382.Google Scholar
Hafner, MS, Sudman, PD, Villablance, FX, Spradling, TA, Demastes, JW and Nadler, SA (1994) Disparate rates of molecular evolution in cospeciating hosts and parasites. Science 265, 1087–1090.Google Scholar
Harbison, CW and Clayton, DH (2011) Community interactions govern host switching with implications for host-parasite coevolutionary history. Proceedings of the National Academy of Sciences USA 108, 9525–9529.Google Scholar
Hopkins, GHE and Clay, T (1952) A Check List of the Genera & Species of Mallophaga. London, United Kingdom: British Museum of Natural History.Google Scholar
Hughes, J, Kennedy, M, Johnson, KP, Palma, RL and Page, RDM (2007) Multiple cophylogenetic analyses reveal frequent cospeciation between Pelecaniform birds and Pectinopygus lice. Systematic Biology 56, 232–251.Google Scholar
Johansson, US and Ericson, PGP (2003) Molecular support for a sister group relationship between Pici and Galbulae (Piciformes sensu Wetmore 1960). Journal of Avian Biology 34, 185–197.Google Scholar
Johnson, KP and Sorenson, MD (1998) Comparing molecular evolution in two mitochondrial protein coding genes (cytochrome b and ND2) in the dabbling ducks (Tribe: Anatini). Molecular Phylogenetics and Evolution 10, 82–94.Google Scholar
Johnson, KP, Weckstein, JD, Witt, CC, Faucett, RC and Moyle, RG (2002) The perils of using host relationships in parasite taxonomy: phylogeny of the Degeeriella complex. Molecular Phylogenetics and Evolution 23, 150–157.Google Scholar
Johnson, KP, Shreve, SM and Smith, VS (2012) Repeated adaptive divergence of microhabitat specialization in avian feather lice. BMC Biology 10, 52.Google Scholar
Jønsson, KA, Irestedt, M, Fuchs, J, Ericson, PGP, Christidis, L, Bowie, RCK, Norman, JA, Pasquet, E and Fjeldså, J (2008) Explosive avian radiations and multi-directional dispersal across Wallacea: evidence from the Campephagidae and other Crown Corvida (Aves). Molecular Phylogenetics and Evolution 47, 221–236.Google Scholar
Lanfear, R, Calcott, B, Ho, SYW and Guindon, S (2012) Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.Google Scholar
Malenke, JR, Johnson, KP and Clayton, DH (2009) Host specialization differentiates cryptic species of feather-feeding lice. Evolution 63, 1427–1438.Google Scholar
Matzke, NJ (2013) Probabilistic historical biogeography: new models for founder-event speciation, imperfect detection, and fossils allow improved accuracy and model-testing. Frontiers of Biogeography 5, 242–248.Google Scholar
Maurer, D and Raikow, RJ (1981) Appendicular myology, phylogeny, and classification of the avian order Coraciiformes (including Trogoniformes). Annals of the Carnegie Museum of Natural History 50, 417–434.Google Scholar
Moyle, RG (2006) A molecular phylogeny of kingfishers (Alcedinidae) with insights into early biogeographic history. The Auk 123, 487–499.Google Scholar
Moyle, RG, Fuchs, J, Pasquet, E and Marks, BD (2007) Feeding behavior, toe count, and the phylogenetic relationships among alcedinine kingfishers (Alcedininae). Journal of Avian Biology 38, 317–326.Google Scholar
Palma, RL (1978) Slide mounting of lice: a detailed description of the Canada balsam technique. New Zealand Entomologist 6, 432–436.Google Scholar
Price, R, Hellenthal, RA, Palma, RL, Johnson, KP and Clayton, DH (2003) The Chewing Lice: World Checklist and Biological Overview. Illinois, USA: Illinois Natural History Survey Special Publication.Google Scholar
Smith, VS, Page, RDM and Johnson, KP (2004) Data incongruence and the problem of avian louse phylogeny. Zoologica Scripta 33, 239–259.Google Scholar
Swofford, DL (2003) PAUP*. Phylogenetic analysis using Parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.Google Scholar
Tendeiro, J (1965) Études sur les Mallophages parasites des Alcédinidés. I. Genre Alcedoecus th. Clay et Meinertzhagen, 1939 et Emersoniella nov. Revista dos Estudos Gerais Universitários de Moçambique 2, 1–92.Google Scholar
Tendeiro, J (1967) Études sur les Mallophages parasites des Alcédinidés. II. Genre Alcedoffula th. Clay et Meinertzhagen, 1939. Considérations finales. Revista dos Estudos Gerais Universitários de Moçambique 4, 195–295.Google Scholar
Tendeiro, J (1983) Nouvelles observations sur les Mallophages (Insecta, Mallophaga) parasites des Alcédinidés. Garcia de Orta, Serie de Zoologia 10, 107–114.Google Scholar
Uchida, S (1948) Studies on the biting-lice (Mallophaga) of Japan and adjacent territories (Suborder Ischnocera Pt. I). Japanese Medical Journal 1, 303–326.Google Scholar
Walther, BA and Clayton, DH (1997) Dust-ruffling: a simple method for quantifying ectoparasite loads of live birds. Journal of Field Ornithology 68, 509–518.Google Scholar
Weckstein, JD (2004) Biogeography explains cophylogenetic patterns in toucan chewing lice. Systematic Biology 53, 154–164.Google Scholar
Weckstein, JD (2005) Molecular phylogenetics of the Ramphastos toucans: implications for the evolution of morphology, vocalizations, and coloration. The Auk 122, 1191–1209.Google Scholar
Zwickl, DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D. dissertation, The University of Texas at Austin. Austin, Texas, USA.Google Scholar
Supplementary material: Image

Catanach et al. supplementary material

Figure S1

Download Catanach et al. supplementary material(Image)
Image 13.3 MB