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 Lice (Phthiraptera): biology i. Diversity • 4,384 spp “chewing lice” (3,508 bird & 402 mammal spp) • 543 spp sucking lice (812 spp mammal) ii. Physical characteristics • wingless, dorsoventrally flattened, 0.3-11mm, 3 nymphal instars • feed on feathers, fur & skin debris (“chewing lice”) or blood • adaptations against host grooming iii. Distribution • mirror host distribution worldwide in virtually every habitat • absent on Chiroptera, Cetacea, Microbiotheria, Monotremata, Notoryctemorphia, Pholidota & Sirenia. iv. Cophylogeny, cospeciation & coevolution Lice (Phthiraptera): taxonomy Chewing Lice Sucking Lice “Mallophaga” (Anoplura) Amblycera Ischnocera Rhynchophthirina Anoplura - 1,350 spp in 6 families - 3,060 spp., # families ? - Just 3 species - 550 spp. in 16 families - Most “primitive” - Widespread, ~90% spp. - On unrelated hosts - Absent from birds suborder on birds - Acquired via shared use - Well studied - More vagile, less host - Avian groups poorly of watering holes? - Greatest medical & specific known - Tiny mandibles present veterinary significance - Widespread on birds - Highly host specific at end of a long rostrum - Vectors of several - 2 fam. South American - Niche restricted pierce hosts thick skin important diseases mammals & marsupials - Mammal infesting - Low prevalence on - 1 fam. on Australasian species of veterinary healthy hosts marsupials significance Lice (Phthiraptera): phylogeny ChewingParasitic Lice Lice Sucking Lice “Mallophaga(Phthiraptera” ) (Anoplura) Psocoptera Amblycera Ischnocera Rhynchophthirina Anoplura Lyal, 1985 (Morphology) Kim & Ludwig, 1982 (Morphology) Suborder Family Genus Anoplura 532 AnopluraPhthiraptera: Rhyn… 3 RhynchophthirinaPhylogenetic resolution, 1996 3,060 Ischnocera Ischnocera 1,344 AmblyceraBirds Amblycera Mammals Suborder Family Genus Anoplura 532 Phthiraptera: Rhyn… 3 Phylogenetic resolution, 2003 3,060 Ischnocera 1,350 Birds Amblycera Mammals 1996 2003 Suborder Family Genus Suborder Family Genus Anoplura 532 541 Rhyn… 3 3 3,060 3,060 Ischnocera 1,344 1,350 Amblycera Amblyceran Families Menoponidae Boopiidae 85 Birds Worldwide & Australasian Marsupials Laemobothriidae Ricinidae Trimenoponidae Protogyropinae 84 Gyropidae South/Central American Gyropinae Rodents & Marsupials Analysed by Marshall, 2003 Grilicolinae from Clay, 1970 (Morphology) Liposcelidae (Psocoptera) Avian Amblycera Liposcelis bostrychophilus 100 Trochiloecetes rupununi Ricinidae 100 93 12 85 Ricinus fringillae - Hummingbirds 3 Trochiliphagus abdominalis Laemobothrion maximum L Laemobothriidae 100 Therodoxus oweni 100 98 100 Boopia tarsata - Falconiforms 8 61 75 Boopidae 15 Paraheterodoxus insignis B 1 61 100 96 Latumcephalum lesouefi/macropus 88 3 99 - Australasian marsupials 9 Paraboopia flava 7 Rediella mirabilis 89 76 Actornithophilus uniseriatus 4 90 Plegadiphilus threskiornis 74 Chapinia robusta 5 Bonomiella columbae 1 62 Pseudomenopon pilosum Dennyus-complex 2 2 Ancistrona vagelli 98 96 Dennyus hirundinis - Birds worldwide 3 Myrsidea victrix A 1 Holomenopon brevithoracicum Eidmanniella pellucida 1 1 Machaerilaemus laticorpus/latifrons Austromenopon-complex 1 Austromenopon crocatum Neomenopon pteroclurus - Aquatic birds 1 Hohorstiella lata M B Osborniella crotophagae 1 52 Eomenopon denticulatum 3 1 Piagetiella bursaepelecani Ciconiphilus quadripustulatus 1 1 Cuculiphilus fasciatus Colpocephalum-complex 2 80 Ardeiphilus trochioxus 57 92 Odoriphila clayae/phoeniculi - Birds worldwide 4 75 1 Psittacomenopon poicephalus 5 51 87 C 1 73 Colpocephalum zebra 3 Comatomenopon elbeli/elongatum Gruimenopon longum 2 Hoazineus armiferus 1 Meromenopon meropis Trinoton anserinum 2 64 Marshall, 2003 57 Menacanthus stramineus Menacanthus/Menopon-cpx. 1 1 Colimenopon urocolius - Birds worldwide 44 genera, 147 char. 2 Somaphantus lusius Amyrsidea ventralis 2 D Menopon gallinae (Morphology) 1 2 Numidicola antennatus First Fossil Louse (Amblycera: Menoponidae) Psocoptera • Collected Eckfeld maar near • Parasite of Anseriformes or Ricinidae Eifel, Germany Charadriiformes • Middle EoceneLae m(Middleobothriida eLutetian, • Crown group position 44.3±0.4 Ma) • Points to a long coevolutionary Boopiidae history with birds • First fossil louse Dennyus • Suggests lice are very old • Completes ordinal- comple xrepresentation • Useful molecular calibration point of fossil insects?Austromenopon - complex • Excellent preservation Menacanthus / • PhylogeneticM affinitiesenopon - co mwithplex modern featherColp olicecephalum - complex Wappler, Smith & Dalgleish , In prep. Ischnoceran Families Suborder Family Genus Anoplura 532 Rhyn… 3 “PhilopteridaeGoniodidae ” Ischnocera 3,060 Ischnocera HeptapsogasteridaeHeptapsogasteridae Trichodectidae Smith,Hopkins 2000 & Clay, 1951 Generic level phylogeny of 1,344 GoniodidaeBirdscf. Eicher, & Heptapsogasteridae 1961 Amblycera (Morphology)21 families Mammals Avian Ischnoceran Phylogeny Haffneria grandis Harrisoniella hopkinsi Paraclisis diomedea PerineusPhiloceanus nigrolimbatus Smith, 2001 Halipeurus pelagicus Philoceanus-complex garrodiae Generic level phylogeny Pseudonirmus gurlti Naubates fuliginosus rd Pelmatocerandra setosa Approx. 1/3 of all ischnoceran genera Ardeicola smithersi Anaticola crassicornis Pectinopygus bassani 51 genera, 138 characters Pectinopygus sulae Aquanirmus australis Ibidoecus plataleae (Morphology) Trabeculus schillingi Craspedonirmus colymbinus QuadracepsSaemundssonia coenocoryphae Docophoroides brevis Saemundssonia-complex desolata Saemundssonia haematopi Podargoecus strigoides Alcedoecus delphax CraspedorrhynchusPhilopterus platystomus Strigiphilus vapidus Sturnidoecus-complex sturni Philopterus ornatus Vernoniella guimarãesi Acidoproctus rostratus Acidoproctus hilli Rallicola lugens Osculotes curtus Osculotes macropoda Coloceras damicorne Campanulotes bidentatus Multiple clades of lice GoniocotesGoniodidae gallinae Goniodes pavonis Goniodes kéleri on the same host Chelopistes guttatus Austrogoniodes waterstoni Strongylocotes angulocapitis DiscocorpusHeptap. c. cephalosus Columbicola columbae SplendoroffulaLipeurus ruwenzorornis Oxylipeurus dentatus Cuclotogaster-complex madagascariensis Lipeurus caponis Degeeriella rufa UpupicolaDegeeriella upupae Lagopoecus affinis Syrrhaptoecus-complex falcatus Neopsittaconirmus borgiolii Paragoniocotes rotundus Brüelia semiannulata Falcolipeurus affulgeus Archolipeurus nandu Geomydoecus (G.) heaneyi Felicola (F.) viverriculae TrichodectesTrichodectidae (T.) melis Bovicola limbatus Damalinia (D.) crenelata 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 Characters Defining Major Ischnoceran Clades PhiloceanusWing Problems with Morphology! -complexLice Smith et al, 2003 • Incongruent with molecularNon- data • Morphological convergencecircumfasciate • Molecular data suggests many of SaemundssoniaHead these pairs are more closely related Lice-complex • Character displacement? Philopterus • Sympatric speciation? -complex Body Circumfasciate GoniodidaeLice CI: 1.0 Heptap. RI: 1.0 LipeurusWing -complex Lice Degeeriella -complex Multiple clades occupy different CI: 0.5 host niches TrichodectidaeRI: 0.95 Rhynchophthirina: Haematomyzidae Suborder Family Genus Anoplura 532 3 Rhynchophthirina 3,060 Ischnocera 1,344 Amblycera 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? Haematomyzus elephantis • Possible cryptic species? ex Asian / African elephant (morphologically identical species on African & Asian elephants) • Specimens hard to come by! Haematomyzus elephantis Haematomyzus hopkinsi Haematomyzus porci Part of Smith, in prep. 51 genera, 76 species 184 characters (Morphology) Anopluran Families Anoplura At least 15 532 distinctAnoplura families Rhyn… 3 3,060 Ischnocera 1,344 Amblycera Anoplura: familial phylogeny • 541spp. in 15 families • Patchily distributed across mammals • Monophyly of all 15 families supported • 3 basal clades • Many lice of host groups (including Primates) paraphyletic Based on Kim, 1988 47 genera, 39 characters (Morphology) Kim’s dataset OUTGROUP “Polyplacidae” 1 re-analysed: “Polyplacidae” 2 “Polyplacidae” 3 Hoplopleuridae • Length=219 (CI=0.26, RI=0.62) “Polyplacidae” 4-12 • Paraphyly of 2 of the 5 families Echinophthiriidae that were not monogenic Enderleinellidae • Just 1 node agrees with Kim’s “Linognathidae” 1 original tree! Neolinognathidae • Only 3 other nodes are “Linognathidae” 2 compatible with Kim’s tree Pedicinidae Pthiridae “Polyplacidae” 13 Ratemiidae Hamophthiriidae Hybophthiridae Pediculidae Pecaroecidae Haematopinidae Kim, 1988 reanalysed Microthoraciidae Strict Consensus Haematomyzus elephantis HaematomyzusHaematomyzidae hopkinsi Haematomyzus porci MicrothoraciusMicrothoraciidae cameli Ratemia squamulata Ratemiidae HamophthiriusHamophthiriidae galeopitheci Hybophthirus notophallus Anoplura: Haematopinus asini Hybophthiridae HaematopinusHaematopinidae suis Pecaroecus javalii Pedicinus ferrisi Pecaroecidae Pedicinus patasPedicinidae phylogeny Pthirus gorillae