The Diversification of Lice: Phylogeny Vincent S. Smith & Kevin P. Johnson

Louse phylogeny four years on… Book lice (Psocoptera) Lice (Phthiraptera) Amblycera Ischnocera Rhynchophthirina Anoplura [ Liposcelis sp.] Chewing Lice “Mallophaga” Sucking Lice (Anoplura) 40+ phylogenies! Now cover 80% of louse genera Mix of molecules & morphology Beginning to reconcile differences Still a long way to go! Some of the biggest studies unpublished

Louse phylogeny four years on… 40+ phylogenies! Now cover 80% of louse genera Mix of molecules & morphology Beginning to reconcile differences [ Liposcelis sp.] Amblycera Ischnocera Rhynchophthirina Anoplura Still a long way to go! Some of the biggest studies unpublished

Australasian Marsupials Amblycera “Feather lice” Australasian Marsupials Birds Worldwide & Rodents & Marsupials South/Central Am. 1,350 spp. in 6 families Grilicolinae Gyropinae Protogyropinae Trimenoponidae Ricinidae Laemobothriidae Boopiidae Menoponidae Liposcelidae (Psocoptera) Gyropidae Widespread on birds Few families on South American mammals & marsupials 85 Boopiidae on Australasian marsupials No new deep-branch phylogenies! Mostly alpha-taxonomic work 84 No extensive molecular trees Clay, 1970

Amblycera “Feather lice” 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 Marshall, 2003 Gruimenopon longum Hoazineus armiferus 44 genera, 147 char. (Morphology) Meromenopon meropis Trinoton anserinum Menacanthus stramineus Colimenopon urocolius Parsimony, Strict consensus Somaphantus lusius Amyrsidea ventralis D Menopon gallinae Numidicola antennatus

Ischnocera “Feather lice” Historically the least studied Philoceanus -complex Goniodidae Degeeriella Trichodectidae Lipeurus Heptap. Saemundssonia Philopterus Historically the least studied Now comparatively well known Extensive molecular & morphological work Haffneria grandis Harrisoniella hopkinsi Paraclisis diomedea 3,104 spp. in an uncertain no. of families Perineus nigrolimbatus Halipeurus pelagicus Philoceanus garrodiae Pseudonirmus gurlti Widespread on birds, 381 spp on mammals Naubates fuliginosus Pelmatocerandra setosa Ardeicola smithersi Anaticola crassicornis Highly host specific (71% on a single host species) 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 Austrogoniodes waterstoni Strongylocotes angulocapitis Discocorpus c. cephalosus Columbicola columbae Splendoroffula ruwenzorornis Oxylipeurus dentatus Cuclotogaster madagascariensis Lipeurus caponis Degeeriella rufa Upupicola upupae Smith, 2001 41 genera, 138 char. (Morphology, parsimony, strict consensus) Lagopoecus affinis Syrrhaptoecus falcatus Neopsittaconirmus borgiolii Paragoniocotes rotundus Brüelia semiannulata Falcolipeurus affulgeus Archolipeurus nandu Geomydoecus (G.) heaneyi Felicola (F.) viverriculae Trichodectes (T.) melis Bovicola limbatus Damalinia (D.) crenelata

Ischnocera “Feather lice” Morphological phylogeny defined by: - multiple clades of lice on the same host Wing CI: 0.5 RI: 0.95 Head Body Circumfasciate Non-circumfasciate CI: 1.0 RI: 1.0 Morphological phylogeny defined by: - shape of the head - body form (wing, head or body louse) A. Circumfasciate B. Non-Circumfasciate N I N II N III Adult C. Wing D. Body E. Head Major clades incongruent with the molecular data!

Ischnocera “Feather lice” Trust me, the same pattern holds! Smith & Johnson, in prep. All ischnceran genera, Adult & Nymphal Morph. Strict Consensus

Rhynchophthirina ? Elephant, warthog & bush pig lice Phylogeny 3 spp. in a single family Confined to relatively unrelated hosts (elephants, warthog & bush pig) Spread via shared use of watering holes? Still chewing lice (telmophages) Phylogeny Only 1 species available for molecular work Haematomyzus elephantis Haematomyzus hopkinsi Haematomyzus porci ? Haematomyzus elephantis ex Asian / African elephant

Anoplura Sucking lice 51 genera, 76 species Rhynchophthirina 540 species in 15 families Hybophthiridae Haematopinidae Ratimidae Confined to mammals (834 host species) Linognathidae Neolinognathidae 50% confined to a single host Microthoracidae Echinophthiridae Blood vessel feeders (solenophages) Hamophthiridae Pecaroecidae Pedicinudae Pthiridae Pediculidae 51 genera, 76 species 184 morphological characters Well supported Consistent with limited mol. data Unpublished Polyplacidae Enderleinellidae Smith, Strict Consensus In Prep. Hoplopleuridae

Anoplura Sucking lice Rodent lice monophyletic Rhynchophthirina Other Anoplura grade into the rodent lice Many monogenic families Hybophthiridae - ungulate lice Haematopinidae Ratimidae All 15 families monophyletic except Polyplacidae Typhlomyophthirus Linognathidae Neolinognathidae Microthoracidae - seal lice Echinophthiridae Strong correlation with host taxonomy Other Anoplura grade into the rodent lice Hamophthiridae Major clades are: - primate lice Pecaroecidae Pedicinudae Pthiridae Pediculidae Polyplacidae Enderleinellidae Hoplopleuridae

Anoplura Sucking lice Focus on Primate lice Reed, Smith et al, 2004 Rhynchophthirina Hybophthiridae Haematopinidae Ratimidae Pediculidae Pthiridae Pedicinidae Reed, Smith et al, 2004 Linognathidae Neolinognathidae Microthoracidae Echinophthiridae Hamophthiridae Pecaroecidae Pedicinudae Pthiridae Pediculidae Polyplacidae Enderleinellidae Hoplopleuridae

Pediculus humanus Human head & body louse morphology Head Lice Body Lice Pediculus capitis De Geer, 1767 Pediculus humanus Linnaeus, 1758 Smaller & darker Larger & lighter Antennae shorter & thicker Antennae longer & slender Middle leg tibial length shorter Middle leg tibial length longer Weak indentations between abdominal segments Below neck. Common in the seams of clothing (especially females), particularly those worn next to the skin (shirts, vests etc.). Males more commonly over garments surface. Restricted to the hair on the scalp, particularly on the nape and in the area behind the ears. Not on the eyebrows or eyelashes. Does not “naturally” vector disease Vectors relapsing fever, trench fever, & epidemic typhus Traditionally considered indistinguishable! Killed no one Killed millions Does not vector a bioterrorism agent Vectors a category B bioterrorism agent

Pediculus humanus Four discriminating characters HdWdth PtWdth TBL TBL: Total Body Length HdWdth HdWdth: Postantennal Head Width LgTibLgth LgTibLgth: 2nd Leg Tibial Length PtWdth PtWdth: Posterior Pterothoracic Width

Pediculus humanus We can morphologically separate head & body lice Discriminant function analysis Function 1 Females Males Function 2 6 4 2 -2 -4 -6 6 4 2 -2 -4 -6 Reed, Smith et al, 2004 1 2 3 3 Pubic Lice 2 Head Lice 1 Body Lice Group Centroids Ungrouped Cases -10 -5 5 10 15 We can morphologically separate head & body lice I want your pill-box specimens!!!

Are these differences present in the molecular data? Pediculus humanus Discriminant function analysis Function 1 Females Males Function 2 6 4 2 -2 -4 -6 6 4 2 -2 -4 -6 Reed, Smith et al, 2004 1 2 3 3 Pubic Lice 2 Head Lice 1 Body Lice Group Centroids Ungrouped Cases -10 -5 5 10 15 Are these differences present in the molecular data?

Questions?