The Diversification of Lice: Phylogeny

Vincent S. Smith& Kevin P. Johnson

Louse phylogeny four years on…

Book lice (Psocoptera)

Lice (Phthiraptera)

AmblyceraAmblycera IschnoceraIschnocera RhynchophthirinaRhynchophthirinaAnopluraAnoplura[ [ Liposcelis Liposcelis

sp.]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• Some of the biggest studies unpublished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…

AmblyceraAmblycera IschnoceraIschnocera RhynchophthirinaRhynchophthirinaAnopluraAnoplura[ [ Liposcelis Liposcelis

sp.]sp.]

• 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• Some of the biggest studies unpublished

Amblycera

“Feather lice”

• No new deep-branch phylogenies!

- 1,350 spp. in 6 families

- Widespread on birds

- Few families on South Americanmammals & marsupials

- Boopiidae on Australasian marsupials

• Mostly alpha-taxonomic work

Clay, 1970

• No extensive molecular trees

84

Grilicolinae

Gyropinae

Protogyropinae

Trimenoponidae

Ricinidae

Laemobothriidae

Boopiidae

Menoponidae

Liposcelidae (Psocoptera)

Gyropidae

Birds W

orldwide &

Australasian M

arsupialsS

outh/Central A

m.

Rodents &

Marsupials

85

Amblycera

“Feather lice”

Laemobothriidae- Falconiforms

Menacanthus/Menopon-cpx.- Birds worldwide

Colpocephalum-complex- Birds worldwide

Austromenopon-complex- Aquatic birds

Dennyus-complex- Birds worldwide

Boopidae- Australasian marsupials

Ricinidae- Hummingbirds

6457

8773

1

1

61

17561

3100 99

9

9385

3

100100

12

100100

15

9688

100 98

7

8

8976

4

3

5

9074

2

1

1 62

29896

11

1

11

1

52

3

2 8057

49275

5 51

13

1

2

1

2

1

2

2

1

12

Trochiloecetes rupununi

Ricinus fringillae

Trochiliphagus abdominalisLaemobothrion maximum

Therodoxus oweni

Boopia tarsataParaheterodoxus insignis

Latumcephalum lesouefi/macropus

Paraboopia flava

Rediella mirabilisActornithophilus uniseriatus

Plegadiphilus threskiornis

Chapinia robustaBonomiella columbae

Pseudomenopon pilosum

Ancistrona vagelli

Dennyus hirundinis

Myrsidea victrix

Holomenopon brevithoracicum

Eidmanniella pellucida

Machaerilaemus laticorpus/latifrons

Austromenopon crocatum

Neomenopon pteroclurus

Hohorstiella lata

Osborniella crotophagaeEomenopon denticulatum

Piagetiella bursaepelecani

Ciconiphilus quadripustulatus

Cuculiphilus fasciatusArdeiphilus trochioxus

Odoriphila clayae/phoeniculi

Psittacomenopon poicephalus

Colpocephalum zebra

Comatomenopon elbeli/elongatum

Gruimenopon longumHoazineus armiferus

Meromenopon meropis

Trinoton anserinum

Menacanthus stramineus

Colimenopon urocolius

Somaphantus lusius

Amyrsidea ventralis

Menopon gallinae

Numidicola antennatus

B

L

M B

C

D

A

Liposcelis bostrychophilus

Marshall, 200344 genera, 147 char. (Morphology)

Parsimony, Strict consensus

Ischnocera

“Feather lice”

- 3,104 spp. in an uncertain no. of families

- Widespread on birds, 381 spp on mammals

- Highly host specific (71% on a single host species)

Columbicola columbae

Austrogoniodes waterstoni

Harrisoniella hopkinsiHaffneria grandis

Paraclisis diomedeaPerineus nigrolimbatusHalipeurus pelagicusPhiloceanus garrodiaePseudonirmus gurltiNaubates fuliginosusPelmatocerandra setosaArdeicola smithersiAnaticola crassicornisPectinopygus bassaniPectinopygus sulaeAquanirmus australisIbidoecus plataleaeTrabeculus schillingiCraspedonirmus colymbinusQuadraceps coenocoryphaeDocophoroides brevisSaemundssonia desolataSaemundssonia haematopiPodargoecus strigoidesAlcedoecus delphaxCraspedorrhynchus platystomusStrigiphilus vapidusSturnidoecus sturniPhilopterus ornatusVernoniella guimarãesiAcidoproctus rostratusAcidoproctus hilliRallicola lugensOsculotes curtusOsculotes macropodaColoceras damicorneCampanulotes bidentatusGoniocotes gallinaeGoniodes pavonisGoniodes kéleriChelopistes guttatus

Strongylocotes angulocapitisDiscocorpus c. cephalosus

Splendoroffula ruwenzorornisOxylipeurus dentatusCuclotogaster madagascariensisLipeurus caponisDegeeriella rufaUpupicola upupaeLagopoecus affinisSyrrhaptoecus falcatusNeopsittaconirmus borgioliiParagoniocotes rotundusBrüelia semiannulataFalcolipeurus affulgeusArcholipeurus nandu

Felicola (F.) viverriculaeGeomydoecus (G.) heaneyi

Trichodectes (T.) melisBovicola limbatusDamalinia (D.) crenelata

Philoceanus-complex

Goniodidae

Degeeriella-complex

Trichodectidae

Lipeurus-complex

Heptap.

Saemundssonia-complex

Philopterus-complex

• Historically the least studied

• Now comparatively well known

• Extensive molecular & morphological work Smith, 2001

41 genera, 138 char. (Morphology, parsimony,

strict consensus)

Ischnocera

“Feather lice”

• 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

- multiple clades of lice on the same host

Wing

CI: 0.5

RI: 0.95

Head

Body

Wing

Circumfasciate

Non-circumfasciate

CI: 1.0RI: 1.0

• Major clades incongruent with the molecular data!

Ischnocera

“Feather lice”

Bovicola limbatusDamalinia (Damalinia) crenelata

Discocorpus c. cephalosusStrongylocotes angulocapitisStrongylocotes complanatusTrichodopeostusHeptapsogaster temporalis

Kelloggia conicepsLamprocorpus hirsutus

Megaginus sordidusMegapeostus asymmetricus

Nothocotus subsimilisOrnicholax robustus

Pectenosoma verrucosaPterocotes aberrans

Rhopaloceras rudimentariusCuclotocephalus extraneus

Physconella kelloggiChelopistes guttatus

Chelopistes meleagridisPachyskelotes orthopleurus

Goniodes pavonisGoniodes kÈleri

Passonomedea hopkinsiColoceras damicorne

Campanulotes comparAuricotes affinis

Goniocotes gallinaePhysconelloides cubanusLabicotes guttatusKodocephalon latumAustrogoniodes waterstoniTrichophilopterus babakotophilusPsittoecus vanzoliniiParagoniocotes rotundusNeopsittaconirmus borgioliiHarrisoniella hopkinsiHaffneria grandisHarrisoniella copeiPerineus nigrolimbatusEpisbates pederiformisBedfordiella unicaHalipeurus pelagicusNaubates fuliginosusPhiloceanus garrodiaePseudonirmus gurltiPelmatocerandra setosaParaclisis diomedeaArdeicola smithersiArdeicola elongata

Fulicoffula longipilaFurnariphilus pageiAnaticola crassicornis

Pseudolipeurus similisPseudophilopterus hirsutus

Psittaconirmus (Psittaconirmus) zinkiEmersoniella bracteata

Hopkinsiella clavigeraRotundiceps cordatus

Trogoniella aequatorialeCuclotogaster madagascariensis

Lipeurus caponisOxylipeurus dentatus

Splendoroffula ruwenzorornisColumbicola columbaeTurturicola salimaliiColilipeurus colius

Colinicola mearnsiSyrrhaptoecus falcatus

Degeeriella rufaLagopoecus affinis

Cotingacola rupicolaeCuculicola atopus

Megapodiella nakataeUpupicola upupae

Buceroemersonia clarkeiAcutifrons chimango

Picicola snodgrassiBuceronirmus deignani

Buceronirmus

Trogoninirmus strigilatusBucorvellus docophorus

CapraiellaCapraiella sabzak

OtidoecusParagoniocotes venezolanus

Paroncophorus javanicusTinamotaecola

Centropodiella borneoensisRhynonirmus scolopacis

Pectinopygus bassaniPectinopygus sulae

Wilsoniella absitaTrabeculus schillingiDocophoroides brevis

Craspedonirmus colymbinusCarduiceps cingulatus

Quadraceps coenocoryphaeSaemundssonia desolataSaemundssonia haematopi

Incidifrons fulicaeMeropoecus meropis

Anatoecus icterodesAlcedoffula alcyonae

Formicaricola willisiAquanirmus australisCraspedorrhynchus platystomus

Strigiphilus vapidusPodargoecus strigoidesAlcedoecus delphaxAegypoecus brevicollisForficuloecus emersoniSturnidoecus sturniCuculoecus latifronsEchinophilopterus protrususPhilopterus ornatusNyctibicola longirostrisPenenirmus auritusCummingsiella ambiguaArdeiphagus cochleariusBizarrifrons magusBuerelius longicepsIncidifrons transpositusCirrophthirius testudinariusLunaceps numeniiFormicaphagus pittasomaeTheresiella geminaMulcticolaTurnicola angustissimusIbidoecus plataleae

Neophilopterus heteropygusAustrophilopterus spinosus

Bucerocophorus pachycnemisVernoniella guimar„esi

Osculotes curtusOsculotes macropoda

Rallicola lugensBr¸elia semiannulata

Brueelia spBBrueelia ornatissima

Pseudocophorus perijanusAcidoproctus rostratusAcidoproctus hilli

Ornithobius goniopleurusBothriometopus macrocnemisEsthiopterum giganteumFalcolipeurus affulgeusArcholipeurus nanduStruthiolipeurus struthionisMeinertzhageniella lataFalcolius elbeliDahlemhornia asymmetricaNesiotinus demersusTrichodectes (Trichodectes) melisFelicola (Felicola) viverriculae

Geomydoecus (Geomydoecus) heaneyi

• Trust me, the same pattern holds!

Smith & Johnson, in prep.

All ischnceran genera, Adult & Nymphal Morph.

Strict Consensus

RhynchophthirinaElephant, warthog & bush pig lice

Haematomyzus elephantis

- 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)

ex Asian / African elephantex Asian / African elephant

• Phylogeny

• Only 1 species available for molecular work

Haematomyzus elephantis

Haematomyzus hopkinsi

Haematomyzus porci?

AnopluraSucking lice

RhynchophthirinaHybophthiridaeHaematopinidaeRatimidae

Linognathidae

NeolinognathidaeMicrothoracidae

Echinophthiridae

HamophthiridaePecaroecidaePedicinudaePthiridaePediculidae

Polyplacidae

Enderleinellidae

Hoplopleuridae

• 51 genera, 76 species

• 184 morphological characters

• Well supported

• Consistent with limited mol. data

• UnpublishedSmith, Strict Consensus

In Prep.

- 540 species in 15 families

- Confined to mammals(834 host species)

- 50% confined to a single host

- Blood vessel feeders (solenophages)

• Other Anoplura grade intothe rodent lice

- ungulate lice- seal lice

• Major clades are:- primate lice

AnopluraSucking lice

• Many monogenic families

RhynchophthirinaHybophthiridaeHaematopinidaeRatimidae

Linognathidae

NeolinognathidaeMicrothoracidae

Echinophthiridae

HamophthiridaePecaroecidaePedicinudaePthiridaePediculidae

Polyplacidae

Enderleinellidae

Hoplopleuridae

• Rodent lice monophyletic

• All 15 families monophyleticexcept Polyplacidae

Typhlomyophthirus

• Strong correlation with hosttaxonomy

• Other Anoplura grade intothe rodent lice

AnopluraSucking lice

RhynchophthirinaHybophthiridaeHaematopinidaeRatimidae

Linognathidae

NeolinognathidaeMicrothoracidae

Echinophthiridae

HamophthiridaePecaroecidaePedicinudaePthiridaePediculidae

Polyplacidae

Enderleinellidae

Hoplopleuridae

• Focus on Primate lice

Pediculidae Pthiridae Pedicinidae

Reed, Smith et al, 2004

Pediculus humanusHuman head & body louse morphology

Head Lice Body LicePediculus humanus Linnaeus, 1758Pediculus capitis De Geer, 1767

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

Restricted to the hair on the scalp, particularly on the nape

and in the area behind the ears. Not on the eyebrows or

eyelashes.

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.

Vectors relapsing fever, trench fever, & epidemic typhus

Does not “naturally” vector disease

Killed millionsKilled no one

Vectors a category B bioterrorism agent

Does not vector a bioterrorism agent

Traditionally considered

indistinguishable!

Pediculus humanusFour discriminating characters

TBLTBL

TBL: Total Body Length

LgTibLgthLgTibLgth

LgTibLgth: 2nd Leg Tibial Length

HdWdthHdWdth

HdWdth: Postantennal Head Width

PtWdthPtWdth

PtWdth: Posterior Pterothoracic Width

Pediculus humanusDiscriminant function analysis

Function 1

Females Males

Fun

ctio

n 2

Group Centroids

Ungrouped Cases

1

23

1

2

3

3 Pubic Lice

2 Head Lice

1 Body Lice-10 -5 0 5 10 15 -10 -5 0 5 10 15

6

4

2

0

-2

-4

-6

6

4

2

0

-2

-4

-6

Reed, Smith et al, 2004

I want your pill-box specimens!!!

We can morphologically separate head & body lice

Pediculus humanus

Function 1

Females Males

Fun

ctio

n 2

Group Centroids

Ungrouped Cases

1

23

1

2

3

3 Pubic Lice

2 Head Lice

1 Body Lice-10 -5 0 5 10 15 -10 -5 0 5 10 15

6

4

2

0

-2

-4

-6

6

4

2

0

-2

-4

-6

Reed, Smith et al, 2004

Are these differences present in the molecular data?

Discriminant function analysis

Questions?