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Lousy Phylogenies: Phthiraptera systematics and the antiquity of lice
Vincent S. Smith Division of Environmental and Evolutionary Biology Institute of Biomedical and Life Sciences Graham Kerr Building University of Glasgow Scotland, UK Intro
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Lice (Phthiraptera): biology
Diversity 4,384 spp “chewing lice” (3,508 bird & 402 mammal spp) 543 spp sucking lice (812 spp mammal) Physical characteristics wingless, dorsoventrally flattened, mm, 3 nymphal instars feed on feathers, fur & skin debris (“chewing lice”) or blood adaptations against host grooming Distribution mirror host distribution worldwide in virtually every habitat absent on Chiroptera, Cetacea, Microbiotheria, Monotremata, Notoryctemorphia, Pholidota & Sirenia. Basic phthirapteran biology and statistics Cophylogeny, cospeciation & coevolution
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Lice (Phthiraptera): taxonomy
Chewing Lice “Mallophaga” Sucking Lice (Anoplura) Amblycera Ischnocera Rhynchophthirina Anoplura - 1,350 spp in 6 families - Most “primitive” suborder - More vagile, less host specific - Widespread on birds - 2 fam. South American mammals & marsupials - 1 fam. on Australasian marsupials - 3,060 spp., # families ? - Widespread, ~90% spp. on birds - Avian groups poorly known - Highly host specific - Niche restricted - Mammal infesting species of veterinary significance - Just 3 species - On unrelated hosts - Acquired via shared use of watering holes? - Tiny mandibles present at end of a long rostrum pierce hosts thick skin - 550 spp. in 16 families - Absent from birds - Well studied - Greatest medical & veterinary significance - Vectors of several important diseases - Low prevalence on healthy hosts
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Lice (Phthiraptera): phylogeny
Parasitic Lice (Phthiraptera) Lyal, 1985 (Morphology) Chewing Lice “Mallophaga” Sucking Lice (Anoplura) Psocoptera Ischnocera Rhynchophthirina Anoplura Amblycera Kim & Ludwig, 1982 (Morphology)
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Phylogenetic resolution, 1996 Rhynchophthirina
Suborder Family Genus Mammals Birds Amblycera Ischnocera Rhyn… Anoplura Phthiraptera: Phylogenetic resolution, 1996 Rhynchophthirina Amblycera Ischnocera Anoplura 532 3 3,060 Principal clades and subordinal phylogeny. Mallophaga issue and 1,344
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Phylogenetic resolution, 2003
Suborder Family Genus Anoplura Phthiraptera: Phylogenetic resolution, 2003 532 Rhyn… 3 3,060 Ischnocera 1,350 Mammals Birds Amblycera
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1996 2003 Genus Family Suborder 3 541 3,060 1,350 Suborder Family
Anoplura 532 Rhyn… 3 3,060 Ischnocera 1,344 Amblycera
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Australasian Marsupials
Amblyceran Families Birds Worldwide & Australasian Marsupials Menoponidae Boopiidae 85 Laemobothriidae Ricinidae Trimenoponidae South/Central American Rodents & Marsupials Gyropidae Protogyropinae 84 Gyropinae Analysed by Marshall, 2003 from Clay, 1970 (Morphology) Grilicolinae Liposcelidae (Psocoptera)
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Avian Amblycera Marshall, 2003 Ricinidae Laemobothriidae Boopidae
- Hummingbirds Liposcelis bostrychophilus 64 57 87 73 1 61 75 3 100 99 9 93 85 12 15 96 88 98 7 8 89 76 4 5 90 74 2 62 52 80 92 51 Trochiloecetes rupununi Ricinus fringillae Laemobothriidae - Falconiforms Trochiliphagus abdominalis Laemobothrion maximum L Boopidae - Australasian marsupials Therodoxus oweni Boopia tarsata Paraheterodoxus insignis B Latumcephalum lesouefi/macropus Paraboopia flava Rediella mirabilis Actornithophilus uniseriatus Plegadiphilus threskiornis Menacanthus/Menopon-cpx. - Birds worldwide Colpocephalum-complex Austromenopon-complex - Aquatic birds Dennyus-complex Chapinia robusta Bonomiella columbae Pseudomenopon pilosum Ancistrona vagelli Dennyus hirundinis Myrsidea victrix A Holomenopon brevithoracicum Eidmanniella pellucida Machaerilaemus laticorpus/latifrons Austromenopon crocatum Neomenopon pteroclurus B Hohorstiella lata M Osborniella crotophagae Eomenopon denticulatum Piagetiella bursaepelecani Ciconiphilus quadripustulatus Cuculiphilus fasciatus Ardeiphilus trochioxus Odoriphila clayae/phoeniculi Psittacomenopon poicephalus C Colpocephalum zebra Comatomenopon elbeli/elongatum Gruimenopon longum Hoazineus armiferus Marshall, 2003 Meromenopon meropis Trinoton anserinum Menacanthus stramineus 44 genera, 147 char. (Morphology) Colimenopon urocolius Somaphantus lusius Amyrsidea ventralis D Menopon gallinae Numidicola antennatus
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First Fossil Louse (Amblycera: Menoponidae)
Collected Eckfeld maar near Eifel, Germany Middle Eocene (Middle Lutetian, 44.3±0.4 Ma) First fossil louse Completes ordinal representation of fossil insects? Excellent preservation Phylogenetic affinities with modern feather lice Parasite of Anseriformes or Charadriiformes Crown group position Points to a long coevolutionary history with birds Suggests lice are very old Useful molecular calibration point P s o c p t e r a M n h u / - m l x R i d L b B A D y C Wappler, Smith & Dalgleish , In prep.
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Ischnoceran Families Ischnocera Birds Mammals Smith, 2000
Suborder Family Genus Smith, 2000 Generic level phylogeny of Goniodidae & Heptapsogasteridae (Morphology) Heptapsogasteridae Goniodidae Ischnocera Anoplura Trichodectidae Heptapsogasteridae “Philopteridae” Hopkins & Clay, 1951 532 Rhyn… 3 3,060 Ischnocera 1,344 Mammals Birds cf. Eicher, families Amblycera
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Avian Ischnoceran Phylogeny
Philoceanus -complex Goniodidae Degeeriella Trichodectidae Lipeurus Heptap. Saemundssonia Philopterus Columbicola columbae Austrogoniodes waterstoni Harrisoniella hopkinsi Haffneria grandis Paraclisis diomedea Perineus nigrolimbatus Halipeurus pelagicus Philoceanus garrodiae Pseudonirmus gurlti Naubates fuliginosus Pelmatocerandra setosa Ardeicola smithersi Anaticola crassicornis Pectinopygus bassani Pectinopygus sulae Aquanirmus australis Ibidoecus plataleae Trabeculus schillingi Craspedonirmus colymbinus Quadraceps coenocoryphae Docophoroides brevis Saemundssonia desolata Saemundssonia haematopi Podargoecus strigoides Alcedoecus delphax Craspedorrhynchus platystomus Strigiphilus vapidus Sturnidoecus sturni Philopterus ornatus Vernoniella guimarãesi Acidoproctus rostratus Acidoproctus hilli Rallicola lugens Osculotes curtus Osculotes macropoda Coloceras damicorne Campanulotes bidentatus Goniocotes gallinae Goniodes pavonis Goniodes kéleri Chelopistes guttatus Strongylocotes angulocapitis Discocorpus c. cephalosus Splendoroffula ruwenzorornis Oxylipeurus dentatus Cuclotogaster madagascariensis Lipeurus caponis Degeeriella rufa Upupicola upupae Lagopoecus affinis Syrrhaptoecus falcatus Neopsittaconirmus borgiolii Paragoniocotes rotundus Brüelia semiannulata Falcolipeurus affulgeus Archolipeurus nandu Felicola (F.) viverriculae Geomydoecus (G.) heaneyi Trichodectes (T.) melis Bovicola limbatus Damalinia (D.) crenelata Smith, 2001 Generic level phylogeny Approx. 1/3rd of all ischnoceran genera 51 genera, 138 characters (Morphology) Multiple clades of lice on the same host
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Characters Defining Major Ischnoceran Clades
A. Circumfasciate Head B. Non-Circumfasciate Head N I N II N III Adult C. Wing Lice D. Body Lice E. Head Lice
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Characters Defining Major Ischnoceran Clades
Wing Lice CI: 0.5 RI: 0.95 Head Body Philoceanus -complex Goniodidae Degeeriella Trichodectidae Lipeurus Heptap. Saemundssonia Philopterus Incongruent with molecular data Morphological convergence Molecular data suggests many of these pairs are more closely related Character displacement? Sympatric speciation? Problems with Morphology! Smith et al, 2003 Circumfasciate Non-circumfasciate CI: 1.0 RI: 1.0 Multiple clades occupy different host niches
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Rhynchophthirina: Haematomyzidae
Suborder Family Genus Rhynchophthirina Anoplura 532 3 3,060 Ischnocera 1,344 Amblycera
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Rhynchophthirina: Haematomyzidae
Just 3 species in 1 family Present on elephants, wart hog & bush pig (perhaps also mammoths?) Monophyly & sister placement with Anoplura well supported Chewing lice (have outwardly opposing mandibles) Pool blood feeders (telmophages) cf vessel feeding Anoplura Spread via shared use of watering holes? Possible cryptic species? (morphologically identical species on African & Asian elephants) Specimens hard to come by! Haematomyzus elephantis ex Asian / African elephant Haematomyzus elephantis Haematomyzus hopkinsi Haematomyzus porci Part of Smith, in prep. 51 genera, 76 species 184 characters (Morphology)
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Anopluran Families Anoplura At least 15 distinct families Anoplura 532
Rhyn… 3 3,060 Ischnocera 1,344 Amblycera
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Anoplura: familial phylogeny 541spp. in 15 families
3 basal clades 541spp. in 15 families Patchily distributed across mammals Many lice of host groups (including Primates) paraphyletic Monophyly of all 15 families supported Based on Kim, 1988 47 genera, 39 characters (Morphology)
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Kim’s dataset re-analysed:
OUTGROUP “Polyplacidae” 1 “Polyplacidae” 2 “Polyplacidae” 3 “Polyplacidae” 4-12 “Linognathidae” 1 “Linognathidae” 2 “Polyplacidae” 13 Paraphyly of 2 of the 5 families that were not monogenic “Polyplacidae” 1 “Polyplacidae” 2 “Polyplacidae” 3 Hoplopleuridae Length=219 (CI=0.26, RI=0.62) “Polyplacidae” 4-12 Echinophthiriidae Enderleinellidae Just 1 node agrees with Kim’s original tree! “Linognathidae” 1 Neolinognathidae Only 3 other nodes are compatible with Kim’s tree “Linognathidae” 2 Pedicinidae Pthiridae “Polyplacidae” 13 Ratemiidae Hamophthiriidae Hybophthiridae Pediculidae Pecaroecidae Haematopinidae Kim, 1988 reanalysed Strict Consensus Microthoraciidae
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Anoplura: phylogeny Why are rodents so lousy?
Haematomyzidae Haematomyzus elephantis Smith, in prep. 51 genera, 76 species 184 characters (Morphology) Haematomyzus hopkinsi Anoplura: phylogeny Microthoraciidae Ratemiidae Hamophthiriidae Hybophthiridae Haematopinidae Pecaroecidae Haematomyzus porci Microthoracius cameli Ratemia squamulata Hamophthirius galeopitheci Hybophthirus notophallus Haematopinus asini Haematopinus suis Pecaroecus javalii Pedicinidae Pthiridae Pediculidae Pedicinus ferrisi Pedicinus patas Pthirus gorillae Pthirus pubis Pediculus schaeffi Pediculus humanus Pediculus mjobergi Pediculus humanus var. americanus “Polyplacidae” 1 Neolinognathidae Scipio aulacodi Scipio tripedatus Linognathidae Neolinognathus sp. Neolinognathus elephantuli Solenopotes muntiacus Prolinognathus aethiopicus Prolinognathus ferrisi Linognathus setosus Linognathus aepycerus Linognathus africanus Echinophthiriidae Latagophthirus rauschi Echinophthirius horridus Lepidophthirus macrorhini Antarctophthirus callorhini Antarctophthirus microchir Proechinophthirus fluctus Proechinophthirus zumpti Enderleinellidae Hoplopleuridae “Polyplacidae” 2 “Polyplacidae” 3 Johnsonpthirus chlorotalpae Johnsonpthirus heliosciuri Lemurphthirus galagus Lemurphthirus stigmosus Linognathoides laeviusculus Sathrax durus Why are rodents so lousy? Why are other mammals relatively louse free cf. birds Good evidence for cophylogeny in some clades Neohaematopinus callosciuri Neohaematopinus inornatus Abrocomaphthirus chilensis Ctenophthirus cercomydis Proenderleinellus calva Polyplax abyssinica Polyplax spinulosa Docophthirus acinetus Eulinognathus denticulatus Haemodipsus leporis Haemodipsus lyriocephalus Lagidiophthirus parvus Fahrenholzia ferrisi Fahrenholzia pinnata Galeophthirus caviae Phthirpediculus brygooi Phthirunculus sumatranus Atopophthirus emersoni Microphthirus uncinatus Enderleinellus osborni Werneckia nigeriensis Comparative studies underway using these trees Hoplopleura acanthopus Paradoxophthirus emarginata Hoplopleura pacifica Hoplopleura irritans Pterophthirus audax Pterophthirus splendida Ancistroplax crocidurae Haematopinoides squamosus Typhlomyophthirus bifoliatus Schizophthirus graphiuri Schizophthirus pleurophaeus
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Louse Molecular Studies
Mitochondrial Nuclear - COI ( bp) - 12S rRNA (450bp) - Cyt. B (450bp) - ND4 (500bp) - EF1-a ( bp) - 18S rRNA (1500+bp) - Wingless, PEPCK, DDC Easy to amplify Limited phylogenetic utility outside families Often restricted to use within closely related genera Hard to amplify Multiple copies RNA alignment issues Utility varies between genes & taxa Need New Genes!
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Relative Substitution Rate
(Mit. COI vs nuc. EF1-a) Data Set COI EF1-a Rate Parameter Ratio (COI:EF1a) Sites all sites pos. 1 pos. 2 pos. 3 1 0.12 129.9 0.018 0.013 0.016 0.41 55.6 76.9 7.5 316.8 Physconelloidinae Lice all sites pos. 1 pos. 2 pos. 3 1 0.15 169.78 0.016 0.039 0.017 0.8 61.5 25.6 8.8 212.2 Columbicola all sites pos. 1 pos. 2 pos. 3 1 0.0001 44.79 0.25 0.20 0.0001 2.49 4.1 5.0 1.0 18.0 aphids
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Louse 12S Secondary Structure
Austrogoniodes cristati Naubates prioni Austrophilopterus subsimilis Austrogoniodes cristati Austrogoniodes waterstoni Oxylipeurus chiniri Campanulotes bidentatus Columbicola columbae Louse 12S Secondary Structure Halipeurus pelagicus Naubates harrisoni Rallicola columbiana mit. 12S rRNA Page et al, 2002
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12S Length Variation Insects vs. Lice Page et al, 2002
Segment 1: 33-33' 20 40 60 80 100 120 140 160 Length insects 210 220 230 240 250 260 270 280 290 300 310 320 1 2 3 4 5 6 7 lice 20 40 60 80 100 120 140 160 Length 5 10 15 25 30 35 45 2 4 6 8 12 Segment 2: 36-38 12S Length Variation 20 40 60 80 100 120 140 160 180 200 Length 15 25 30 35 45 50 55 65 70 75 85 2 4 6 8 10 12 14 Segment 3: 38'-39' Segment 5: 34'-33' 120 100 80 60 40 20 Length 10 9 8 7 6 Insects vs. Lice 5 4 3 2 1 Page et al, 2002 35 40 45 50 55 60 65 70 75 80 Length
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Louse Mitochondrial Genome
cox1 cox3 nad1 cob nad4 nad4L nad2 nad3 nad5 cox2 rrnL rrnS atp6 atp8 nad6 S2 L2 KNAY QV PT DIFS1 CMWERII GL1 Gene arrangement of Heterodoxus macropus (Amblycera) cox1 cox2 atp8 atp6 cox3 nad3 nad5 nad4 nad4L nad6 cob nad2 rrnL rrnS L2 KD G H ARNS1EF TP V S2 L1 IQM WCY Inferred gene arrangement of ancestral insect Adapted from Shao, Campbell & Barker, 2001
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Louse Molecular Studies
Mitochondrial Nuclear - EF1-a ( bp) - 18S rRNA (1500+bp) - Wingless, PEPCK, DDC Hard to amplify Multiple copies RNA alignment issues Utility varies between genes & taxa - COI ( bp) - 12S rRNA (450bp) - Cyt. B (450bp) - ND4 (500bp) Easy to amplify Limited phylogenetic utility outside families Often restricted to use within closely related genera Need New Genes!
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Louse Nuclear Genes What Not to do! 350 bp single copy EF1-a
RHYN… ANOPLURA What Not to do! 350 bp single copy EF1-a Limited phylogenetic utility above families ISCHNOCERA AMBLYCERA Cruickshank et al, 2001
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Phylogenetic Utility 18S rRNA
Smith et al, 2003
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Conclusions… Ongoing Questions…
Much recent progress on basal phthirapteran phylogeny Monophyly of suborders well supported Complex pattern of host-louse relationships Distinctive molecular evolution in lice Incongruence between molecules & morphology Ongoing Questions… To what extent do lice cospeciate with their hosts? Why are some hosts more lousy than others? How old are the major louse clades? Are Phthiraptera truly paraphyletic?
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Acknowledgements Collaboration Funding Stephen Barker Dale Clayton
Tom Ford Kevin Johnson Rod Page Isabel Marshall David Reed Funding Wellcome Trust, UK Natural Environment Research Council, UK
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Pairwise ML Corrected Distances for 3rd Sites
(Nuclear EF1-a against Mit. COI) 300 200 ML Corrected Divergences (COI 3rd Positions) 100 Slope approximates relative rate Around 1000:1 !!! 0.1 0.2 0.3 0.4 0.5 0.6 ML Corrected Divergences (EF1-a 3rd Positions) Johnson et al, 2003
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18S – not a panacea for basal louse Phylogeny!
Trogiomorph Psocoptera Trogiomorph Psocoptera Liposcelis sp. Amblycera Ischnocera Liposcelis sp. Ischnocera Amblycera Uncorrected NJ Anoplura Bayesian Anoplura 0.1 0.1
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