abdad franch & monteiro.2007.biogeography and evolution of amazonian mines

57Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 102(Suppl. I): 57-69, 2007

Biogeography and evolution of Amazonian triatomines(Heteroptera: Reduviidae): implications for Chagas disease

surveillance in humid forest ecoregions

Fernando Abad-Franch/*/+, Fernando A Monteiro**

Instituto Leônidas & Maria Deane-Fiocruz Amazônia, Rua Teresina 476, 69057-070 Manaus, AM, Brasil *PMBU-ITD, LondonSchool of Hygiene and Tropical Medicine, London, UK **Instituto Oswaldo Cruz-Fiocruz, Rio de Janeiro, RJ, Brasil

An ecological-evolutionary classification of Amazonian triatomines is proposed based on a revision oftheir main contemporary biogeographical patterns. Truly Amazonian triatomines include the Rhodniini, theCavernicolini, and perhaps Eratyrus and some Bolboderini. The tribe Rhodniini comprises two major lineages(pictipes and robustus). The former gave rise to trans-Andean (pallescens) and Amazonian (pictipes) speciesgroups, while the latter diversified within Amazonia (robustus group) and radiated to neighbouring ecoregions(Orinoco, Cerrado-Caatinga-Chaco, and Atlantic Forest). Three widely distributed Panstrongylus species prob-ably occupied Amazonia secondarily, while a few Triatoma species include Amazonian populations that occuronly in the fringes of the region. T. maculata probably represents a vicariant subset isolated from its parentallineage in the Caatinga-Cerrado system when moist forests closed a dry trans-Amazonian corridor. Thesediverse Amazonian triatomines display different degrees of synanthropism, defining a behavioural gradientfrom household invasion by adult triatomines to the stable colonisation of artificial structures. Anthropogenicecological disturbance (driven by deforestation) is probably crucial in the onset of the process, but the fact thatonly a small fraction of species effectively colonises artificial environments suggests a role for evolution at theend of the gradient. Domestic infestation foci are restricted to drier subregions within Amazonia; thus, popula-tions adapted to extremely humid rainforest microclimates may have limited chances of successfully colonisingthe slightly drier artificial microenvironments. These observations suggest several research avenues, from the use ofclimate data to map risk areas to the assessment of the synanthropic potential of individual vector species.

Key words: Triatominae - ecology - evolution - biogeography - Chagas disease - Amazonia

Financial support: the UNDP-World Bank-WHO TDR SpecialProgramme, Fiocruz, CNPq, Fapeam, the ECLAT Network. Thispaper is contribution no. 4 of the Research Programme on Infec-tious Disease Ecology in the Amazon (RP-IDEA) of the InstitutoLeônidas & Maria Deane.+Corresponding author: [email protected] 4 July 2007Accepted 3 September 2007

AMAZONIA

The Amazon is the largest subregion within the Neo-tropical biogeographical region. It encompasses 13 bio-geographical provinces and over 40 ecoregions (cf.Olson et al. 2001, WWF 2001, Morrone 2006) (TablesI-III, Fig. 1). The greater Amazon biome (~ 6.5 millionkm2) is comprised of many diverse biotic communities.The Amazon River fluvial network, with over 10 thou-sand tributaries, irrigates > 5 million km2 of tropicalforests (moist and dry, terra firme and seasonallyflooded, lowland and montane) and the open formations,Campinas, Campinaranas, and anthropic landscapes thatconstitute the ecological mosaic of Amazonia. Consideredas a whole, the Amazon is the most biologically diversebiome on Earth – as measured by the absolute number ofspecies recorded in each region (Mittermeier et al. 2003).

From a wider (biogeographical, ecological, and evo-lutionary) perspective, the Amazon complex may be con-sidered to include certain physically contiguous systemsand ecoregions with which it shares key aspects of itshistorical biogeography. The most important among theseregions are the Orinoco and Tocantins/Araguaia basins,the Guyanan Shield highlands, and the eastern slopes ofthe northern-central Andes (including the Peruvian SelvaAlta, the Yungas, and the inter-Andean valleys drainingtowards the Amazon-Orinoco system). In Brazil, both thedrier ecoregions of the Cerrado and the Caatinga (particu-larly the relatively humid forests along riverbanks and moun-tain ranges) and the moist Atlantic Forests harbour animaland plant communities that reveal their ancient biogeo-graphical-evolutionary relationship with Amazonia.

Many factors and processes have been invoked toexplain the regional patterns of biological diversifica-tion. Whatever the weight of their relative contributions,geological substrate heterogeneity, climatic fluctuationsand habitat fragmentation, hydro- and oro-graphicalvicariant events, dispersal and adaptive radiation, localextinction, genetic drift or coevolution all have prob-ably played a role. It seems safe enough to admit that thehistorical evolution of this huge biogeographical com-plex offered a vast number of ecological-adaptive op-portunities (and constraints) for organic diversificationby natural selection of variants, thus shaping the system-atic relationships among contemporary lineages (cf.Rossetti et al. 2005). It is therefore obvious that a soundunderstanding of the biology of Amazonian organisms

58 Evolution of Amazonian triatomines • F Abad-Franch, FA Monteiro

must take into account not only their systematic struc-turing and current ecological associations, but also thehistorical (evolutionary) aspects of the different lineagesand of the environments where they originated and di-versified.

THE TRIATOMINAE OF AMAZONIA

The true number of Amazonian triatomine speciesremains probably unknown. Records from the Amazon-Orinoco-Tocantins/Araguaia systems, the Guyana Shield,and the eastern Andean foothills include no less than 27recognised species (with a few further taxa probablypresent in some subregions) grouped into nine generaand five tribes: Rhodniini (ten Rhodnius and at least onePsammolestes species), Triatomini (four Triatoma,three Panstrongylus, and two Eratyrus species) Caverni-colini (two Cavernicola species), Alberproseniini (twoAlberprosenia species), and Bolboderini (at least twoBelminus and one Microtriatoma species) (see TablesII, III). It is however very likely that many further taxa

Fig. 1: province biogeography of the Neotropical region and the distribu-tion of Rhodnius spp. Numbers indicate biogeographical provinces (af-ter Morrone 2006) specified in Table I. Green areas correspond to theAmazon province. The red line in Central America suggests the northernlimit of natural (sylvatic) R. pallescens populations. The red line acrossprovince number 13 suggests the southern limit of Amazonian Rhodniuspopulations. Grey areas in Mesoamerica indicate the distribution of in-troduced R. prolixus populations (* = Chiapas province). The orangearea corresponds to the Paraná Forest province, where R. domesticuslikely occurs.

occur in the Amazon that have not yet been formally de-scribed. Lineages composed of small, dull-coloured,canopy-living organisms (like those within the last threetribes we have just mentioned) are the most obvious can-didates to encompass undescribed species. Other likelycandidates are those ‘species’ considered to be eitherbiologically very variable and/or extensively distributed,which might conceal species complexes. The recent find-ing of moderately divergent mitochondrial haplotypesin phenotypically indistinguishable populations of thewidespread R. robustus (Monteiro et al. 2003) indicatesthat the biological diversity of well-known triatominetaxa is also higher than previously thought. The growinguse of DNA barcoding techniques in arthropod taxonomyis revealing how underestimated is species richness inbiodiversity inventories based on classical phenotypicapproaches (see for instance Miller 2007).

Even a superficial biogeographical appraisal suggeststhat the many triatomine species reported to occur inAmazonia fall into distinct categories. Some must beconsidered as truly Amazonian, while others evolved else-where and occupied the region secondarily. Among theformer, some radiated to neighbouring ecoregions anddiversified (speciating in some cases), while others re-mained endemic to their areas of origin. Among the lat-ter, some are populations of widely distributed species,others are found in the ecotones along the fringes of theregion, and a few represent isolated populations derivedfrom currently allopatric stem lineages.

In an attempt to put forward a coherent account ofthe systematic, ecological, and behavioural diversity ofAmazonian triatomines, we underscore in this paper theimportance of adopting a biogeographical and evolution-ary stance – which might be broadly interpreted asphylogeographical. Following this rationale, we presentan approximation to the historical biogeography and evo-lution of the main triatomine lineages known to occur inthe greater Amazon, classifying them accordingly, anddiscuss how this view may foster a biologically soundunderstanding of synanthropic behavioural trendsamong these vectors.

A PHYLOGEOGRAPHICAL CLASSIFICATION OFAMAZONIAN TRIATOMINES

The draft classification we propose here is based onan approximation to the evolutionary origins and diver-sification patterns of the Amazonian lineages within theRhodniini, Panstrongylus and Triatoma, but we will alsoconsider other groups. The judgments underlying ourproposal are biogeographical, ecological, and evolution-ary; we made an effort to avoid excess speculation bytrying to focus on taxon groups that can be safely con-sidered to be monophyletic, even if they are not recog-nised as formal systematic units in some cases.

Truly Amazonian Triatominae - This group includesall the lineages whose centre of origin, diversification,and dispersal (giving rise to currently sympatric,parapatric or allopatric derived taxa) was probably thecore region of moist tropical forests corresponding tocontemporary Amazonia.

59Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 102(Suppl. I), 2007

The paradigmatic example of this group is the tribeRhodniini, an assemblage of arboricolous triatomines(most of them associated with palm trees) grouped intotwo genera – Psammolestes and Rhodnius (Lent &Wygodzinsky 1979, Galvão et al. 2003). While the phy-logenetic relationships of many triatomine tribes andgenera remain problematic, the Rhodniini are consid-

TABLE I

Biogeography of the Neotropical region and the distribution of Rhodnius spp.

Region Subregion Dominion Province Numbera

Neotropical Caribbean Mesoamerican Mexican Pacific CoastMexican GulfChiapasEastern Central America 15Western Panamanian Isthmus 16

Antillean Yucatán PeninsulaBahamaCubaCayman IslandsJamaicaHispaniolaPuerto RicoLesser Antilles

Northwestern South American Chocó 17Maracaibo 18Magdalena 19Trinidad and TobagoVenezuelan Coastc 20Venezuelan Llanosc 21CaucaGalápagos IslandsWestern Ecuador 22Arid Ecuador 23Tumbes-Piura 24

Amazonian Guyana 1Humid Guyana 2Napo 3Imeri 4Roraima 5Amapá 6Várzea 7Ucayali 8Madeira 9Tapajós-Xingu 10Pará 11Yungas 12Pantanal 13

Chacoan Cerradoc 25Caatingac 26Chacoc

Pampa

Paraná Brazilian Atlantic Forest 27Paraná Forestb 28Araucaria Forest

Grey cells correspond to provinces with records of naturally occurring Rhodnius species and populations; a: numbers as in Fig. 1;b: likely occurrence of natural Rhodnius populations; c: recorded occurrence of Psammolestes spp.

ered monophyletic beyond controversy (Hypša et al.2002, De Paula et al. 2005). The two genera within thetribe are however paraphyletic, with Psammolestes spe-cies sharing a common ancestor with R. robustus and itsclosest relatives (Monteiro et al. 2000, 2002).

The 19 species within the tribe Rhodniini have beenclassified into two main groups (Schofield & Dujardin


TABLE II

Biogeography of the triatomines from the greater Orinoco (Northwestern South American biogeographical dominion)

Biogeographic provincea Hydrographic basin(s) Ecoregionb Species of Triatominae

Maracaibo Lake Maracaibo Maracaibo dry forests Rhodnius prolixus, R. robustus (I), R. pictipes,R. neivai, Triatoma dimidiata?, T. maculata,T. nigromaculata, Panstrongylus geniculatus,P. rufotuberculatus, Eratyrus mucronatus,E. cuspidatus, Alberprosenia goyovargasi

Catatumbo moist R. prolixus, R. robustus (I)?, R. pictipes,forests T. dimidiata?, T. maculata?, P. geniculatus,

P. rufotuberculatus, E. mucronatus, E. cuspidatus,Cavernicola pilosa?

Guajira/Barranquilla R. prolixus, R. neivai, T. dimidiata?,xeric scrub T.a maculata, P. geniculatus, P. rufotuberculatus?,

E. mucronatus?, E. cuspidatus?

Paraguana xeric scrub R. prolixus, R. robustus (I)?, R. pictipes?, R. neivai,Psammolestes arthuri, T. dimidiata, T.a maculata,T. nigromaculata, P. geniculatus, P rufotubercula-tus, E mucronatus?, E cuspidatus

Orinoco/Magdalena Cordillera Oriental R. prolixus, R. robustus (I), R. pictipes, R. dalessandroi?,(Northern Colombia) montane forests T. dimidiata (Colombia), T. maculata?, P. geniculatus,

P. rufotuberculatus?, E. mucronatus, E. cuspidatus,C. pilosa, Belminus rugulosus?

Venezuelan Venezuelan coastal La Costa xeric R. prolixus, R. robustus (I)?, R. pictipes?, P. arthuri,Coast basins shrublands T. dimidiata, T. maculata, T. nigromaculata,

P. geniculatus, P.s rufotuberculatus, E. mucronatus,E. cuspidatus, B. pittieri, B. rugulosus

Cordillera La Costa R.s prolixus, R. robustus (I)?, R. pictipes, T. dimidia-montane forests ta?, T. maculata?, P. geniculatus, P. rufotuberculatus?,

E. mucronatus?, Microtriatoma trinidadensis,B. pittieri?, B. rugulosus?

Lara/Falcón dry forests R. prolixus, R. robustus (I), R. neivai, T. dimidata?, T.maculata, T. nigromaculata?, P. geniculatus, P.rufotuberculatus, E. mucronatus, E.cuspidatus

Trinidad basins Trinidad and Tobago E. mucronatus, M. trinidadensismoist forests

Paraguana xeric scrub R. prolixus, R. robustus (I)?, R. pictipes?, R. neivai,P. arthuri, T. dimidiata, T. maculata, T. nigromaculata,P. geniculatus, P.s rufotuberculatus, E. mucronatus?,E. cuspidatus

Araya and Paria R. prolixus, R. robustus (I)?, T. dimidiata?,xeric scrub T. maculata?, P. geniculatus?, P. rufotuberculatus?,

E. mucronatus?, E. cuspidatus?

Venezuelan Llanos Orinoco Llanos R. prolixus, R. robustus (I), R. pictipes,R. dalessandroi, P. arthuri, T. dimidiata, T. maculata,T. nigromaculata, P. geniculatus, P. rufotuberculatus,E. mucronatus, E. cuspidatus, C. pilosa,B. rugulosus?, M. trinidadensis?

Apure/Villavicencio R. prolixus, R. robustus (I), R. pictipes?, P. arthuri, T.dry forests dimidiata, T. maculata, T. nigromaculata,

P. geniculatus, P. lignarius??, P. rufotuberculatus,E. mucronatus, E. cuspidatus, C. pilosa, B. rugulosus?

Orinoco Delta R. prolixus?, R. robustus (I, IV)?, R. pictipes,swamp forests T. dimidiata?, T. maculata?, T. nigromaculata??,

P. geniculatus, P. rufotuberculatus?, P. lignarius?,E. mucronatus?, M. trinidadensis

Orinoco wetlands R. prolixus?, R. robustus (I, IV)?, R. pictipes?,P. geniculatus?, P. lignarius?, P. rufotuberculatus?,E. mucronatus?, M. trinidadensis?

a: after Morrone (2006); b: after WWF (2001); ? indicates the species is probably present in the ecoregion; ?? indicates the species ispossibly present in the ecoregion; roman numerals refer to R. robustus genotypic groups defined after Monteiro et al. (2003); triatominerecords follow Carcavallo et al. (1999) and Galvão et al. (2003).


TAB

LE

III

Bio

geog

raph

y of

the

tria

tom

ines

from

the

Am

azon

ian

subr

egio

n

Bio

geog

raph

ic p

rovi

ncea

Hyd

rogr

aphi

c ba

sin(

s)E

core

gion

bSp

ecie

s of

Tri

atom

inae

Nap

oA

maz

onas

Caq

uetá

moi

st fo

rest

sR

hodn

ius

robu

stus

(II

), R

. pi

ctip

es,

R.

bret

hesi

, P

anst

rong

ylus

gen

icul

atus

,P.

s ru

fotu

berc

ulat

us,

P. l

igna

rius

?, E

raty

rus

muc

rona

tus,

Cav

erni

cola

pil

osa,

Mic

rotr

iato

ma

trin

idad

ensi

s

Nap

o m

oist

fore

sts

R. r

obus

tus

(II)

, R. s

p.(r

obus

tus

linea

ge),

R. p

icti

pes,

P. g

enic

ulat

us,

P. r

ufot

uber

cula

tus?

, P. l

igna

rius

(an

d li

gnar

ius-

herr

eri

inte

rmed

iate

for

ms)

,E

. m

ucro

natu

s, C

. pi

losa

Solim

ões/

Japu

rá m

oist

fore

sts

R.

robu

stus

(II

), R

. pi

ctip

es,

R.

bret

hesi

?, P

. ge

nicu

latu

s, P

. ru

fotu

berc

ulat

us,

P. l

igna

rius

, E

. m

ucro

natu

s, C

. pi

losa

, M

. tr

inid

aden

sis?

, B

elm

inus

per

uvia

nus?

Cor

dille

ra O

rien

tal m

onta

neR

. pro

lixu

s, R

. rob

ustu

s (I

, II?

), R

. pic

tipe

s, R

. dal

essa

ndro

i??,

T. d

imid

iata

??,

fore

sts

(sou

ther

n th

ird)

P. g

enic

ulat

us,

P. r

ufot

uber

cula

tus?

, E

. m

ucro

natu

s, E

. cu

spid

atus

, C

. pi

losa

,B

. ru

gulo

sus?

?

Eas

tern

Cor

dille

raR

. rob

ustu

s (I

I), R

hodn

ius

sp.(

robu

stus

line

age)

?, R

. pic

tipe

s, T

. car

rion

i, T.

ven

osa,

Rea

l mon

tane

fore

sts

P. g

enic

ulat

us?,

P.

rufo

tube

rcul

atus

?, P

.lign

ariu

s?,

B.

peru

vian

us?

Am

azon

as/O

rino

coN

egro

/Bra

nco

moi

st fo

rest

sR

. pr

olix

us?,

R.

robu

stus

(I)

, R.

pict

ipes

, R. b

reth

esi,

T. m

acul

ata?

, P.

geni

cula

tus,

P. r

ufot

uber

cula

tus?

, P.

lig

nari

us?,

E.m

ucro

natu

s, C

. pi

losa

, M

. tr

inid

aden

sis

Ori

noco

Apu

re/V

illav

icen

cio

R. p

roli

xus?

, R. r

obus

tus

(I),

R. p

icti

pes?

, Psa

mm

oles

tes

arth

uri,

T. d

imid

iata

?,dr

y fo

rest

s (s

outh

ern

limit)

T. m

acul

ata,

T.

nigr

omac

ulat

a?,

P. g

enic

ulat

us,

P. l

igna

rius

??,

P. r

ufot

uber

cula

tus,

E.

muc

rona

tus,

E.

cusp

idat

us,

C.

pilo

sa,

B.

rugu

losu

s??

Imer

iA

maz

onas

Japu

rá/S

olim

ões-

Neg

roR

. rob

ustu

s (I

I, I

V, *

), R

. pi

ctip

es, R

. br

ethe

si, P

. ge

nicu

latu

s, P

. ru

fotu

berc

ulat

us,

moi

st fo

rest

sP.

lig

nari

us,

Era

tyru

s m

ucro

natu

s, C

. pi

losa

, M

. tr

inid

aden

sis

Neg

ro/B

ranc

o m

oist

fore

sts

R.

prol

ixus

?, R

. ro

bust

us (

I), R

. pi

ctip

es, R

. bre

thes

i, T.

mac

ulat

a?, P

. ge

nicu

latu

s,P.

ruf

otub

ercu

latu

s?,

P. l

igna

rius

?, E

. m

ucro

natu

s, C

. pi

losa

, M

. tr

inid

aden

sis

Caq

uetá

moi

st fo

rest

sR

. ro

bust

us (

II),

R.

pict

ipes

, R

. br

ethe

si,

P. g

enic

ulat

us,

P. r

ufot

uber

cula

tus,

P.

lign

ariu

s,E

. m

ucro

natu

s, C

. pi

losa

, M

. tr

inid

aden

sis

Solim

ões/

Japu

rá m

oist

fore

sts

R.

robu

stus

(II

), R

. pi

ctip

es,

R.

bret

hesi

?, P

. ge

nicu

latu

s, P

. ru

fotu

berc

ulat

us,

P. l

igna

rius

, E

. m

ucro

natu

s, C

. pi

losa

, M

. tr

inid

aden

sis?

, B

. pe

ruvi

anus

?

Rio

Neg

ro C

ampi

nara

nas

R.

robu

stus

(I,

II?

), R

.s p

icti

pes,

R.

bret

hesi

, P.

gen

icul

atus

?, P

. ru

fotu

berc

ulat

us?,

P. l

igna

rius

?, E

. m

ucro

natu

s?,

C.

pilo

sa?,

M.

trin

idad

ensi

s?

Am

azon

as/O

rino

coG

uyan

an H

ighl

ands

R.

prol

ixus

?, R

. ro

bust

us (

I), R

. pi

ctip

es,

T. m

acul

ata,

T.

nigr

omac

ulat

a?, P

. ge

nicu

latu

s,m

oist

fore

sts

P. r

ufot

uber

cula

tus,

P.

lign

ariu

s, E

. m

ucro

natu

s, C

. pi

losa

, M

. tr

inid

aden

sis?

Guy

ana

Am

azon

as/O

rino

coG

uyan

an H

ighl

ands

R.

prol

ixus

?, R

. ro

bust

us (

I), R

. pi

ctip

es,

T. m

acul

ata,

T.

nigr

omac

ulat

a?, P

. ge

nicu

latu

s,m

oist

fore

sts

P. r

ufot

uber

cula

tus,

P.

lign

ariu

s, E

. m

ucro

natu

s, C

. pi

losa

, M

. tr

inid

aden

sis?

Ori

noco

Lla

nos

R.

prol

ixus

, R

. ro

bust

us (

I), R

. pi

ctip

es,

R.

dale

ssan

droi

, P

sam

mol

este

s ar

thur

i,T.

dim

idia

ta,

T. m

acul

ata,

T.

nigr

omac

ulat

a, P

. ge

nicu

latu

s, P

. ru

fotu

berc

ulat

us,

E.

muc

rona

tus,

E.

cusp

idat

us,

C.

pilo

sa,

B.

rugu

losu

s?,

M.

trin

idad

ensi

s?

Ori

noco

-Coa

stal

Guy

anan

bas

ins

Tepu

isT.

mac

ulat

a??,

P.

geni

cula

tus?

?, E

. m

ucro

natu

s??,

C.

pilo

sa??

Hum

id G

uyan

aG

uyan

an c

oast

al b

asin

sG

uian

an m

oist

fore

sts

R.

prol

ixus

?, R

. ro

bust

us (

IV),

R.

pict

ipes

, R.

amaz

onic

us, R

. pa

raen

sis,

T.

dim

idia

ta?,

T. m

acul

ata,

T.

nigr

omac

ulat

a??,

P.

geni

cula

tus,

P.

rufo

tube

rcul

atus

, P.

lig

nari

us,

�


Bio

geog

raph

ic p

rovi

ncea

Hyd

rogr

aphi

c ba

sin(

s)E

core

gion

bSp

ecie

s of

Tri

atom

inae

E.

muc

rona

tus,

C.

pilo

sa?,

M.

trin

idad

ensi

s

Para

mar

ibo

swam

p fo

rest

sR

. ro

bust

us (

IV)?

, R

. pi

ctip

es?,

R.

amaz

onic

us??

, R

. pa

raen

sis?

?, P

. ge

nicu

latu

s?,

P. r

ufot

uber

cula

tus?

, P.

lig

nari

us?,

E.

muc

rona

tus?

, C

. pi

losa

?, M

. tr

inid

aden

sis?

Ori

noco

Ori

noco

Del

ta s

wam

p fo

rest

sR

. pro

lixu

s?, R

. rob

ustu

s (I

V, I

?), R

. pic

tipe

s, T

. dim

idia

ta?,

T. m

acul

ata?

,T.

nig

rom

acul

ata?

?, P

. ge

nicu

latu

s, P

. ru

fotu

berc

ulat

us?,

P.

lign

ariu

s?,

E.

muc

rona

tus?

,M

. tr

inid

aden

sis

Ror

aim

aA

maz

onas

Uat

umã-

Tro

mbe

tas

R. r

obus

tus

(I, I

V),

R.

pict

ipes

, R.

amaz

onic

us, R

. br

ethe

si??

, R.

para

ensi

s,m

oist

fore

sts

P. g

enic

ulat

us,

P. r

ufot

uber

cula

tus,

P.

lign

ariu

s, E

. m

ucro

natu

s, C

. pi

losa

, C

. le

nti,

M.

trin

idad

ensi

s?

Guy

anan

sav

anna

sR

. pr

olix

us??

, R.

robu

stus

(I)

?, R

. pi

ctip

es?,

T.

mac

ulat

a, P

. ge

nicu

latu

s,P.

ruf

otub

ercu

latu

s??,

E.

muc

rona

tus?

, C

. pi

losa

?

Am

apá

Am

azon

asU

atum

ã-T

rom

beta

sR

. rob

ustu

s (I

, IV

), R

. pi

ctip

es, R

. am

azon

icus

, R.

bret

hesi

??, R

. pa

raen

sis,

moi

st fo

rest

sP.

gen

icul

atus

, P.

ruf

otub

ercu

latu

s, P

. li

gnar

ius,

E.

muc

rona

tus,

C.

pilo

sa,

C.

lent

i,M

. tr

inid

aden

sis?

Mar

ajó

várz

ea fo

rest

sR

. ro

bust

us (

IV),

R.

pict

ipes

, R

. am

azon

icus

?, R

. pa

raen

sis?

, P.

gen

icul

atus

,P.

ruf

otub

ercu

latu

s?,

P. l

igna

rius

, E

. m

ucro

natu

s?,

C.

pilo

sa,

M.

trin

idad

ensi

s?,

Alb

erpr

osen

ia m

alhe

iroi

, B

. la

port

ei

Gur

upa

várz

eaR

. ro

bust

us (

IV)?

, R

. pi

ctip

es?,

R.

amaz

onic

us?,

R.

para

ensi

s?,

P. g

enic

ulat

us?,

P. r

ufot

uber

cula

tus?

, P.

lig

nari

us?,

E.m

ucro

natu

s?,

C.

pilo

sa?,

M.

trin

idad

ensi

s?

Guy

anan

sav

anna

sR

. pr

olix

us??

, R

. ro

bust

us (

IV)?

, R

. pi

ctip

es?,

T.

mac

ulat

a??,

P.

geni

cula

tus,

P. r

ufot

uber

cula

tus?

, E

. m

ucro

natu

s?,

C.

pilo

sa?

Uca

yali

Am

azon

asU

caya

li m

oist

fore

sts

R.

robu

stus

(II

), R

. pi

ctip

es,

P. g

enic

ulat

us,

P. r

ufot

uber

cula

tus?

, P.

lig

nari

us,

E.

muc

rona

tus,

C.

pilo

sa,

M.

trin

idad

ensi

s?,

B.

peru

vian

us?

Iqui

tos

várz

eaR

. ro

bust

us (

II),

R.

pict

ipes

, P.

gen

icul

atus

, P.

ruf

otub

ercu

latu

s?,

P. l

igna

rius

?,E

. m

ucro

natu

s?,

C.

pilo

sa?,

M.

trin

idad

ensi

s?,

B.p

eruv

ianu

s?

Mad

eira

Am

azon

asM

adei

ra/T

apaj

ós m

oist

fore

sts

R. r

obus

tus

(II,

III

, IV

), R

. pic

tipe

s, R

. sta

li, R

. bre

thes

i?, P

. ter

tius

?, P

. gen

icul

atus

,P.

ruf

otub

ercu

latu

s, P

. li

gnar

ius,

E.m

ucro

natu

s, C

. pi

losa

, M

. tr

inid

aden

sis?

Puru

s/M

adei

ra m

oist

fore

sts

R. r

obus

tus

(II,

IV

, III

?), R

. pic

tipe

s, R

. sta

li?,

R. b

reth

esi?

, P. g

enic

ulat

us,

P. r

ufot

uber

cula

tus?

, P.

lig

nari

us,

E.

muc

rona

tus,

C.

pilo

sa,

M.

trin

idad

ensi

s?

Juru

á/Pu

rus

moi

st fo

rest

sR

. ro

bust

us (

II),

R.

pict

ipes

, R

. br

ethe

si??

, P.

gen

icul

atus

, P.

ruf

otub

ercu

latu

s,P.

lig

nari

us,

E.

muc

rona

tus,

C.

pilo

sa,

M.

trin

idad

ensi

s?

Puru

s vá

rzea

R.

robu

stus

(II

), R

. pi

ctip

es,

R.

bret

hesi

?, P

. ge

nicu

latu

s, P

. ru

fotu

berc

ulat

us?,

P. l

igna

rius

?, E

. m

ucro

natu

s?,

C.

pilo

sa?,

M.

trin

idad

ensi

s?

Mon

te A

legr

e vá

rzea

R.

robu

stus

(II

, IV

), R

; pi

ctip

es,

P. g

enic

ulat

us,

P. r

ufot

uber

cula

tus?

, P.

lig

nari

us?,

E.

muc

rona

tus?

, C

. pi

losa

?, M

. tr

inid

aden

sis?

Vár

zea

Am

azon

asPu

rus

várz

eaR

. ro

bust

us (

II),

R.

pict

ipes

, R

. br

ethe

si?,

P.

geni

cula

tus,

P.

rufo

tube

rcul

atus

?,P.

lig

nari

us?,

E.

muc

rona

tus?

, C

. pi

losa

?, M

.trin

idad

ensi

s?

Mon

te A

legr

e vá

rzea

R.

robu

stus

(II

, IV

), R

. pi

ctip

es, R

. am

azon

icus

?, R

. pa

raen

sis?

, P.

gen

icul

atus

,P.

ruf

otub

ercu

latu

s?,

P. l

igna

rius

?, E

. m

ucro

natu

s?,

C.

pilo

sa?,

M.

trin

idad

ensi

s?

Iqui

tos

várz

eaR

. ro

bust

us (

II),

R.

pict

ipes

, P.

gen

icul

atus

, P.

ruf

otub

ercu

latu

s?,

P. l

igna

rius

?,�


Bio

geog

raph

ic p

rovi

ncea

Hyd

rogr

aphi

c ba

sin(

s)E

core

gion

bSp

ecie

s of

Tri

atom

inae

E.

muc

rona

tus?

, C

. pi

losa

?, M

. tr

inid

aden

sis?

, B

. pe

ruvi

anus

?

Tapa

jós-

Xin

guA

maz

onas

Tapa

jós/

Xin

gu m

oist

fore

sts

R. r

obus

tus

(III

), R

. pic

tipe

s, R

. bre

thes

i, P.

ter

tius

?, P

. gen

icul

atus

,P.

ruf

otub

ercu

latu

s?,

P. l

igna

rius

, E

. m

ucro

natu

s?,

C.

pilo

sa?,

M.

trin

idad

ensi

s?

Xin

gu/T

ocan

tins-

Ara

guai

aR

. ro

bust

us (

III)

, R

. pi

ctip

es,

R.

bret

hesi

?, P

. ge

nicu

latu

s, P

. ru

fotu

berc

ulat

us,

moi

st fo

rest

sP.

lig

nari

us,

E.

muc

rona

tus,

C.

pilo

sa,

M.

trin

idad

ensi

s, A

lber

pros

enia

mal

heir

oi?,

B.

lapo

rtei

?

Gur

upa

várz

eaR

. ro

bust

us (

IV)?

, R

. pi

ctip

es?,

R.

amaz

onic

us?,

R.

para

ensi

s?,

P. g

enic

ulat

us?,

P. r

ufot

uber

cula

tus?

, P.

lig

nari

us?,

E.

muc

rona

tus?

, C

. pi

losa

?, M

. tr

inid

aden

sis?

Mat

o G

ross

o tr

opic

alR

. rob

ustu

s (I

II, I

I?),

R.

pict

ipes

?, R

. ne

glec

tus?

, P.s

ter

tius

, P.

geni

cula

tus?

,dr

y fo

rest

sP.

ruf

otub

ercu

latu

s?,

P. l

igna

rius

?, C

.a p

ilos

a, M

. tr

inid

aden

sis

Par

áTo

cant

ins-

Ara

guai

a/To

cant

ins-

Ara

guai

a/M

aran

hão

R. r

obus

tus

(III

, IV

), R

. pic

tipe

s, R

. mil

esi,

R. n

egle

ctus

, R. p

arae

nsis

, P. t

erti

us?,

coas

tal b

asin

sm

oist

fore

sts

P.

geni

cula

tus,

P.

rufo

tube

rcul

atus

?, P

. li

gnar

ius,

E.

muc

rona

tus,

C.

pilo

sa?,

A. m

alhe

iroi

?, B

. lap

orte

i?

Pind

aré-

Parn

aíba

Mar

anhã

o B

abaç

u fo

rest

sR

. rob

ustu

s (I

V),

R.

pict

ipes

, R.

mil

esi?

, R.

negl

ectu

s, R

. na

sutu

s, P

. gen

icul

atus

,P.

ruf

otub

ercu

latu

s?,

P. l

igna

rius

, E

.muc

rona

tus?

?, C

. pi

losa

?

Mar

anhã

o co

asta

l bas

ins

Nor

thea

ster

n re

stin

gas

No

data

Yun

gas

Am

azon

asPe

ruvi

an Y

unga

sR

. rob

ustu

s (I

I), R

. pic

tipe

s, R

. ecu

ador

iens

is??

(pr

imar

ily

tran

s-A

ndea

n), T

. car

rion

i,P.

gen

icul

atus

, P. r

ufot

uber

cula

tus,

P. l

igna

rius

her

reri

, P. c

hina

i??

(pri

mar

ily

tran

s-A

ndea

n),

E.

muc

rona

tus?

, E

. cu

spid

atus

?, C

. pi

losa

?, B

. pe

ruvi

anus

Bol

ivia

n Y

unga

sR

. ro

bust

us (

II),

R.

stal

i, P.

gen

icul

atus

, P.

ruf

otub

ercu

latu

s?,

P. l

igna

rius

?,E

. m

ucro

natu

s?,

C.

pilo

sa?,

M.

trin

idad

ensi

s

And

ean

Yun

gas

P. c

oreo

des,

P.

geni

cula

tus,

P.

rufo

tube

rcul

atus

?

Am

azon

as-M

arañ

ónM

arañ

ón d

ry fo

rest

sR

. rob

ustu

s (I

I)?,

R. e

cuad

orie

nsis

(pr

imar

ily t

rans

-And

ean)

, T. c

arri

oni,

P. g

enic

ulat

us?,

P. r

ufot

uber

cula

tus,

P. l

igna

rius

her

reri

, P. c

hina

i (pr

imar

ily tr

ans-

And

ean)

,E

. m

ucro

natu

s?,

E.

cusp

idat

us??

, B

. pe

ruvi

anus

Pant

anal

Am

azon

asM

adei

ra/T

apaj

ós m

oist

fore

sts

R. r

obus

tus

(II,

III

, IV

), R

. pic

tipe

s, R

. sta

li, R

. bre

thes

i?, P

. ter

tius

?, P

. gen

icul

atus

,P.

ruf

otub

ercu

latu

s, P

. li

gnar

ius,

E.

muc

rona

tus,

C.

pilo

sa,

M.

trin

idad

ensi

s?

Puru

s/M

adei

ra m

oist

fore

sts

R. r

obus

tus

(II,

IV

, III

?), R

. pic

tipe

s, R

. sta

li?,

R. b

reth

esi?

, P. g

enic

ulat

us,

P. r

ufot

uber

cula

tus?

, P.

lig

nari

us,

E.

muc

rona

tus,

C.

pilo

sa,

M.

trin

idad

ensi

s?

Sout

hwes

tern

Am

azon

ian

R. r

obus

tus

(II)

, R

. pi

ctip

es, R

. st

ali,

P. c

oreo

des?

, P.

geni

cula

tus,

moi

st fo

rest

sP.

ruf

otub

ercu

latu

s, P

. li

gnar

ius,

E.

muc

rona

tus,

C.

pilo

sa,

M.

trin

idad

ensi

s?,

B.

peru

vian

us?

Mon

te A

legr

e vá

rzea

R.

robu

stus

(II

), R

. pi

ctip

es,

R.

stal

i??,

P.

geni

cula

tus,

P.

rufo

tube

rcul

atus

?,P.

lig

nari

us?,

E.

muc

rona

tus?

, C

. pi

losa

?, M

. tr

inid

aden

sis?

, B

. pe

ruvi

anus

??

Iqui

tos

várz

eaR

. ro

bust

us (

II),

R.

pict

ipes

, P.

gen

icul

atus

, P.

ruf

otub

ercu

latu

s?,

P. l

igna

rius

?,E

. m

ucro

natu

s?,

C.

pilo

sa?,

M.

trin

idad

ensi

s?,

B.

peru

vian

us?

Mat

o G

ross

o tr

opic

alR

.s r

obus

tus

(III

, II?

), R

. pi

ctip

es?,

R.

negl

ectu

s?, P

. te

rtiu

s, P

. ge

nicu

latu

s?,

dry

fore

sts

P. r

ufot

uber

cula

tus?

, P.

lig

nari

us?,

C.

pilo

sa,

M.

trin

idad

ensi

s

Ben

i sav

anna

sR

. ro

bust

us (

II)?

, R.

pict

ipes

?, R

. st

ali,

P. t

erti

us?,

P.

geni

cula

tus,

P.

rufo

tube

rcul

atus

,E

. m

ucro

natu

s?,

M.

trin

idad

ensi

s?�


1999). The ‘pictipes group’ includes species from boththe eastern (pictipes, stali, brethesi, paraensis, andamazonicus) and western (pallescens, colombiensis, andecuadoriensis) sides of the Andes. The members of the‘robustus group’ (robustus, prolixus , nasutus,neglectus, milesi, dalessandroi, domesticus, and thePsammolestes) are all cis-Andean [only R. neivai, en-demic to the dry forests of the eastern Maracaibo bio-geographical province, includes geographically re-stricted trans-Andean populations]. However, the verypresence of two biogeographically well-defined groupsof species (cis- and trans-Andean) has also been inter-preted as signalling a basal evolutionary split within thetribe. Mitochondrial rDNA sequence analyses failed toprovide convincing evidence to uphold any of these twocompeting hypotheses (Hypša et al. 2001, De Paula etal. 2007), but mt cytochrome b gene (cytb) genealogiestend to support the existence of two major, monophyl-etic groups: the ‘pictipes’ and the ‘robustus’ lineages(Abad-Franch & Monteiro 2005 and unpublished data).

Several lines of evidence suggest a palaeo-Amazo-nian origin of the Rhodniini. First, only three of theknown extant species are entirely trans-Andean (seeabove). Eleven of the 16 cis-Andean species have beenrecorded in the greater Amazon (including the Orinocoand Tocantins/Araguaia systems); the best studied amongthese (particularly R. robustus) are genetically very di-verse entities probably encompassing several, recentlydiversified cryptic taxa (Monteiro et al. 2003). Thesedata suggest that the core biogeographical region of thetribe would correspond to contemporary Amazonia. Theclose ecological association between most Rhodniusspecies and palm trees may reflect a long (perhaps up to> 90 million years) process of parallel evolution of bothlineages (Gaunt & Miles 2002). Palm trees first evolvedin moist tropical forests of the Gondwana floral prov-ince during the warm late Cretaceous, and occupied drierlife zones secondarily (cf. Cox & Moore 2000). Assum-ing that the Rhodniini followed their palm ecotopesalong this evolutionary pathway, it may be concluded thatthey also appeared for the first time in humid tropicalforests. The exclusively Neotropical range of extant lin-eages suggests that they probably evolved in the moistEquatorial forests of western Gondwana. The averagecytb sequence divergences between the more widely dis-tributed representatives of the tribe (R. pictipes and R.robustus) exceeds 20% (FA-F & FAM, unpublished data),suggesting that their most recent common ancestor livedin the Miocene [10-12 million years ago (Mya); assum-ing a rate of 2.3% pairwise sequence divergence permillion years (Brower 1994)], when flooded moist for-ests (similar to contemporary várzea) prevailed in theAmazon (cf. Hoorn 1994).

The diversification of these palaeo-Amazonian an-cestors followed diverse patterns. Mt cytb sequence datasuggest that R. pictipes and R. pallescens-colombiensisshare a common ancestor that lived in the late Miocene(~ 6 Mya), just before the Andes increased their maxi-mum altitude to over 4000m (Cox & Moore 2000, Abad-Franch et al. 2003). The time since divergence of R.ecuadoriensis from its Colombian relatives (R. pal-B

ioge

ogra

phic

pro

vinc

eaH

ydro

grap

hic

basi

n(s)

Eco

regi

onb

Spec

ies

of T

riat

omin

ae

Am

azon

as/P

aran

áC

hiqu

itani

a dr

y fo

rest

sR

. ro

bust

us (

II?)

, R

. st

ali,

P. c

oreo

des,

P.

geni

cula

tus,

P.

rufo

tube

rcul

atus

,E

. m

ucro

natu

s?,

M.

trin

idad

ensi

s?

Para

ná/A

maz

onas

Pant

anal

R.

robu

stus

(II

?), R

. st

ali,

P. t

erti

us?,

P.

core

odes

?, P

. ge

nicu

latu

s, P

. ru

fotu

berc

ulat

us?,

E.

muc

rona

tus

Para

ná/A

maz

onas

/C

erra

doR

. rob

ustu

s (I

I, I

II?)

?, R

. sta

li?,

R. n

egle

ctus

, P. t

erti

us, P

. cor

eode

s, P

. gen

icul

atus

,A

ragu

aia-

Toca

ntin

sP.

s ru

fotu

berc

ulat

us?

a: a

fter

Mor

rone

(200

6); b

: aft

er W

WF

(200

1); ?

indi

cate

s th

e sp

ecie

s is

pro

babl

y pr

esen

t in

the

ecor

egio

n; ?

? in

dica

tes

the

spec

ies

is p

ossi

bly

pres

ent i

n th

e ec

oreg

ion;

rom

an n

umer

als

refe

rto

R. r

obus

tus

geno

typi

c gr

oups

def

ined

aft

er M

onte

iro

et a

l. (2

003)

; *in

dica

tes

the

pres

ence

of a

rece

ntly

dis

cove

red

mt c

ytb

geno

type

in th

is e

core

gion

(see

text

). T

riat

omin

e re

cord

s fo

llow

Car

cava

llo

et a

l. (1

999)

and

Gal

vão

et a

l. (2

003)

.


lescens and R. colombiensis) (~ 5 Mya) roughly coin-cides with the uplift of the Andes in the Pliocene. A plau-sible explanation to the current distribution of the mem-bers of the Pacific Rhodnius lineage would thereforecombine the effects of adaptive radiation and vicariance.An ancestral population perhaps reached the western sideof the (then low) Andes range during the late Mioceneby migrating from the eastern Orinoco plains; subse-quently, the rise of the Andes during the Pliocene splitthat population into two main clades: the northern (nowColombian) cluster, comprising the ancestral forms ofR. pallescens and R. colombiensis, and an isolated pocketin the south, which adapted to new ecotopes and eventuallygave rise to R. ecuadoriensis (Abad-Franch et al. 2003).

The bulk of the diversification of the AmazonianRhodnius lineages (the cis-Andean group derived fromthe ‘pictipes lineage’ and all the known representativesof the ‘robustus lineage’) probably took place in syn-chrony with the orographic-hydrographic changes and theclimatic fluctuations (with profound local and regionalecological impact) that took place in the late Plioceneand the Pleistocene (cf. Rossetti et al. 2005). Duringinterglacial periods for instance, moist forests expandedbeyond their current limits, allowing for the colonisationof new regions by representatives of the tribe. Some ofthem dispersed towards presently arid or semi-aridecoregions, particularly the Colombian-VenezuelanLlanos to the north and the Brazilian Cerrado and Caatingato the south. In some cases, these ancestral dispersingpopulations established ecological associations with dryforest palm species (Copernicia tectorum-R. prolixus,C. prunifera-R. nasutus, Acrocomia spp.-R. neglectus),while in others they reached new territories followingMauritia flexuosa gallery forests or adapting to pro-tected microenvironments (Psammolestes-bird nests).The genetic consequences of Amazonian moist forestfragmentation during the Pleistocene can be traced inthe relationships between R. robustus mt cytbhaplotypes, with at least four moderately distinct vari-ants (~ 2.3-4% sequence divergence) occurring acrossthe greater Amazon (Monteiro et al. 2003, Abad-Franch& Monteiro 2005; see Fig. 2). The phylogeographic hy-pothesis proposed by Monteiro et al. (2003) to explainthe diversification of these Amazonian R. robustus cladeswould receive further support if R. pictipes populations(with similar overall geographic distribution) were shownto present comparable patterns of genetic structuring.The question has not been thoroughly examined so far.

R. domesticus is probably the living representativeof an ancient coastal lineage that remained isolated fromits Amazon ancestors when the humid forest corridorslinking Amazonia with the Brazilian Atlantic Forest dis-appeared. A similar process of early isolation might havegiven rise to R. neivai in the northern xeric forests andshrublands of the Maracaibo biogeographical province.

The apparent ecological specialisation of someRhodnius and Psammolestes species may have alsoplayed a role in the diversification of the tribe. Thus, R.brethesi seems to be tightly associated with Leopoldiniapiassaba palms, and it has been suggested that the dis-tribution of R. stali closely matches that of Attalea

phalerata palms in the southwestern fringe of the Ama-zon biome (Matías et al. 2003). R. paraensis is thoughtto be associated with an arboreal rodent of the genusChrysurus, and a similar process of host specialisation,in this case involving birds (mainly Furnariidae), mayhave resulted in the diversification of the Psammolestesfrom an ancestral form belonging to the ‘robustus lineage’.

Some less well-studied triatomine taxa also appearto have evolved in the Amazon moist forests. These in-clude the Cavernicolini, the genus Eratyrus, Microtri-atoma trinidadensis, and perhaps the Belminus-Parabelminus lineage. The phylogenetic affinities andevolutionary origins of these groups have not been thor-oughly investigated; our statements about them, basedon ecological-biogeographic information, are thereforeonly tentative. The two known Cavernicola species livein close association with cave- and hollow tree-dwell-ing bat colonies (Barrett 1991). C. pilosa is a widelydistributed species; while records exist from severalextra-Amazonian ecoregions, the core of its distribu-tion lies apparently within Amazonia. C. lenti has onlybeen reported to occur in a geographically restricted areawithin the Uatumã-Trombetas moist forests of the Bra-zilian Amazon. These data suggest an Amazonian originof the tribe, followed by passive, host-mediated spread

Fig. 2: approximate province biogeography of Rhodnius robustus geno-types [defined after Monteiro et al. (2003) and Pavan & Monteiro (2007)].A red dot in the central Amazon indicates the collection site of the new R.robustus genotype (a member of the R. robustus I - R. prolixus clade)cited in the text. Biogeographical provinces as in Fig. 1 and Table I.


of the pilosa lineage. E. mucronatus occurs in hollowtrees throughout the Amazon-Orinoco basins, whereascis-Andean E. cuspidatus populations seem restrictedto Northern Venezuela, also suggesting an Amazoniancommon ancestor of the genus. The biogeographical pat-tern of M. trinidadensis (which occurs in a ring encom-passing the Amazon-Orinoco fringes) could be inter-preted as the result of a centrifugal adaptive radiation ofpopulations of Amazonian origin. A prediction of thishypothesis is that the species should be present in cen-tral Amazonia, but no records existed from the area(Carcavallo et al. 1999, Galvão et al. 2003) until the re-cent collection of a male specimen in the Japurá/Solimões-Negro moist forests (Brazilian central Ama-zon) (FA-F, unpublished). The Belminus-Parabelminuslineage has also several representatives in the Amazonas-Orinoco system, but some species are trans-Andean andsome (the Parabelminus) are endemic to the BrazilianAtlantic Forests; it is therefore difficult to put forward ahypothesis about its origins, and they could well fit alsoin the second subdivision of our classification.

Widely distributed lineages - Several triatominespecies reported from the greater Amazon belong towidely distributed lineages whose centre of origin anddiversification lies outside the region. They probablyoccupied Amazonian ecoregions secondarily; while somewere awarded formal specific status, others are simplyconsidered geographical populations of their parentalspecies. Representatives of this second major class allbelong to the genus Panstrongylus, but the Belminus-Parabelminus lineage could have followed similar evo-lutionary pathways.

Amazonian Panstrongylus populations belong tothree species (P. geniculatus, P. lignarius-herreri, andP. rufotuberculatus) that seem to be related to theMesoamerican Triatomini lineage (Marcilla et al. 2002).The ancestors of this lineage evolved several millionyears before the complete closure of the Panama Isth-mus, ~ 3 Mya (Bargues et al. 2000, Cox & Moore 2000),suggesting a secondary occupation of South America bytheir descendants. P. geniculatus is a widely distributedand phenotypically diverse triatomine species. It survivesin arid life zones by exploiting highly protected, humidunderground microhabitats (particularly armadillo bur-rows). This strategy probably helped it disperse towardsthe Amazon across the dry regions of northern SouthAmerica. Once in the moist Amazon forests, P. geni-culatus colonised less protected environments such ashollow trees, dead logs, palm tree crowns, and, sporadi-cally, peridomestic pigsties. P. lignarius belongs to asmall monophyletic group of arboricolous species thatoccupy moist tropical forests in Central America (P.humeralis) and the Amazon (P. lignarius). A synan-thropic population (P. herreri, recently synonymisedwith lignarius) lives in the dry forests of the Marañónvalley in Northeastern Peru. It probably represents aparapatric derivative of lowland Amazonian populationsknown as P. lignarius. Sporadic records suggest that P.rufotuberculatus is also present throughout the greaterAmazon. Its extensive geographic range, its phylogenetic

affinities with Mesoamerican Triatomini, and its eco-logical plasticity all suggest a secondary spread of thisspecies across Amazonian ecoregions.

Relict species: the strange case of T. maculata - T.maculata is the only representative of the genus Triatomawith abundant native populations within the greater Ama-zon. It is probably also the only representative of thebiogeographically South American Triatoma lineage thatoccurs north of the parallel 10ºS. Its presumed sisterspecies (T. pseudomaculata) and its closest relatives(T. wygodzinskyi and T. arthurneivai) occur in theCaatinga and the Cerrado. The vicariant distribution ofthese species in dry ecoregions north and south of themoist Amazon forests was interpreted as the result ofpassive dispersal of nymphs by migratory birds. Thishypothesis seems to have been refuted by recentallozyme data showing large genetic distances separat-ing T. maculata from T. pseudomaculata (as opposedto the very small differences detected between the lat-ter and T. wygodzinskyi; dos Santos et al. 2007). Theseresults are compatible with a complex phylogeographicscenario in which an ancestral Triatoma population oc-cupied dry corridors linking the arid Brazilian North-east region with the savannahs of the Orinoco system.The ancestors of extant T. maculata populations becameisolated from their southern relatives when the moisttropical forest matrix closed those dry corridors, set-ting out the process of independent evolution we can nowtrace with genetic markers. The diversification of thesouthern lineage is reflected in the several species thathave been formally described, while the northern cladeis still considered monospecific (comprising only T.maculata). A thorough assessment of the genetic and phe-notypic variability within T. maculata may therefore be pre-dicted to reveal much more diversity than would be expectedamong populations of a recently dispersed species. In sum-mary, contemporary T. maculata populations probablyrepresent an old relict from the times when tropical dryforest corridors traversed Amazonia from north to south.

In the fringes of the Amazon - A few populations ofprimarily Andean triatomine species have been recordedin montane foothill forests that belong to the greaterAmazon biome. This is the case of T. carrioni in Ecua-dor (where T. venosa also occurs) and Northern Peru(Abad-Franch et al. 2001, Cuba Cuba et al. 2002). T.nigromaculata also belongs to the carrioni-venosa-dispar lineage, and is therefore probably of Andean ori-gin. Its range includes a large portion of the VenezuelanOrinoco and coastal basins and the Guyanan highlands,where it preferentially occurs in dry ecoregions. P. chinaiand R. ecuadoriensis, both primarily trans-Andean, oc-cur in the upper (Andean) stretches of some Peruvianvalleys that drain into the Amazon. R. colombiensis, oc-casionally included in checklists of Amazoniantriatomines, is endemic to the Magdalena Valley dry for-ests, and therefore exclusively trans-Andean. Recordsof T. sordida and T. infestans in the Bolivian Amazonmay be the result of mislabelling or may represent pas-sively dispersed individuals carried beyond their naturalbiogeographic range. All the species in this class, per-


haps with the exception of T. nigromaculata, seem how-ever to have limited tolerance to the general ecologicalconditions of the core Amazon region, and may there-fore be predicted to remain confined to relatively small,peripheral areas.

Artificial introductions - T. rubrofasciata is atropicopolitan species that occupies artificial environ-ments in harbour cities, generally in association with rats.Its presence in Belém or São Luís, the main sea harboursof the Brazilian Amazon region, is therefore hardly sur-prising. The most likely explanation, given the phyloge-netic affinities, geographical range, and habits of thisspecies, is that Amazonian populations were introducedby sea trade into the region. Domestic populations ofother, more dangerous species are also candidates toartificial introduction.

Particularly worrying is the case of R. prolixus, nowthe main vector of human Chagas disease, which is na-tive to the drier forests of the Orinoco basin system(mainly the Llanos) but may also colonise humid envi-ronments. There are sparse records of this species inseveral Amazonian localities (in Brazil, the Guyanas, andColombia), and the southern limits of sylvatic R.prolixus populations have not been defined so far. Theircapacity to adapt to palm tree genera with wide distribu-tion throughout Amazonia (such as Attalea) is well docu-mented, and may signal a potential for southward dis-persal. In the Venezuelan-Colombian Llanos, sylvatic R.prolixus from Attalea palms contribute to the infesta-tion and reinfestation of houses and peridomestic struc-tures. Finally, preliminary mt cytb data have revealed theexistence of a third cryptic taxon within the monophyl-etic group composed of R. prolixus and R. robustus I(sensu Monteiro et al. 2003). It occurs in Attalea palmsof the central Brazilian Amazon (FAM & FA-F, unpub-lished data). The presence of these genotypes in Amazo-nian moist forests configures a potentially dangeroussituation that should be carefully monitored. IntroducedT. infestans populations reached the southeastern limitsof the Brazilian Amazon, but were subsequently elimi-nated. In northeastern Bolivia, some of the regions wheresylvatic populations are common include inter-Andeanvalleys that drain into the Amazon. Both empirical fielddata and eco-geographical models (Gorla 2002) suggesthowever that T. infestans has a limited ability to thrivein the warm and humid climate conditions of most Ama-zonian forest regions. T. dimidiata natural populations areon the contrary present in many, extremely diverseecoregions (from the Yucatán Peninsula to Ecuador), in-cluding both dry and moist forest environments, and couldperhaps colonise artificial structures in the Amazon.

THE ECOLOGICAL AND EVOLUTIONARY CONTEXTOF SYNANTHROPIC TRENDS IN AMAZONIANTRIATOMINES

Amazonian triatomines are essentially sylvatic. Epi-demiological and entomological data suggest howeverthat sporadic contact between Trypanosoma cruzi-in-fected vectors and humans, even if relatively infrequent,occurs throughout the region. Most cases of T. cruzitransmission to humans are mediated by adult triatomines

that invade houses, attack forest workers or contami-nate food-processing equipment (see Aguilar et al. 2007,this volume). On the other hand, several native triatominespecies colonise artificial environments in well-definedmicro-regions. These different degrees of synanthropismmay be interpreted as a behavioural gradient starting withthe mere invasion of a house by an adult adventitiousbug and eventually leading to the stable infestation ofhuman dwellings by large breeding vector colonies. Un-derstanding the relative roles of ecological and evolu-tionary factors in the shaping of this gradient may sub-stantially improve our ability to predict which speciesare likely to progress along the gradient, and may alsohelp identify weak (and strong) links that could (or couldnot) be used as the targets of disease prevention strate-gies. We now present a tentative partition of such eco-logical and evolutionary components based on our over-view of the historical biogeography of Amazoniantriatomines.

Ecological factors - Random events and ecologicalpressure linked to anthropic landscape transformationare probably key factors in the initial portion of thebehavioural gradient leading to synanthropism. The dy-namics of land occupation in the Amazon moist forestecoregions illustrate particularly well this process. Ini-tially, forest clearance leads to a reduction of wild ver-tebrate populations; a pattern of selective deforestationin which palm trees are kept in peridomestic environ-ments is commonplace. Palm triatomine populations(mainly Rhodnius species) are probably subject to highmortality during this phase, but do not disappear com-pletely. The palms become suitable shelters for oppor-tunistic marsupials and rodents (Didelphis marsupialis,Rattus spp.) that proliferate in human-modified environ-ments. Residual triatomine populations may take advan-tage of this situation, using these (now abundant) bloodsources to recover and eventually build-up large colo-nies in some palms (Abad-Franch et al. 2005). When thesystem nears its carrying capacity, a reduced availabilityof blood per individual results in adult starved triatominesfrequently flying into nearby houses. Humans, palms,adventitious triatomines and opportunistic mammals (of-ten infected by T. cruzi) closely coexist in anthropic land-scapes throughout the Amazon, increasing disease trans-mission risk (Aguilar et al. 2007, this volume).

However, it is evident that only a small fraction ofthe triatomines that reach human dwellings founds vi-able domestic breeding colonies. Most die off; a fewmay perhaps lie eggs, but their offspring only reach thereproductive stage on very rare occasions. It is conceiv-able that the (relatively few) triatomine populations withthe capacity of thriving in artificial microenvironmentsmay have acquired (through natural selection) some char-acteristics that distinguish them from others of the samelineage that cannot establish domestic colonies.

Evolutionary factors - Natural selection of any traitthat could favour specifically the adaptation of atriatomine population to artificial ecotopes (built byhumans) can only have operated during the last 10 to 12thousand years, which is the approximate age of the first


known human settlements in the Americas. Such an eventseems extremely unlikely in the absence of a very strongand persistent directional selective pressure. We mayenvisage, however, that a set of traits exists that, havingbeen selected over millions of years for other reasons,confers the ability to exploit domestic habitats to thepopulations that possess it. Populations of the same lin-eage lacking those traits would fail to permanently in-fest households. In such a case, we would expect thatonly a few populations among all the possible candidateswithin a given lineage (those that possess the set of traitsin question) be able to successfully colonise artificialenvironments. The biogeographical-evolutionary sce-nario we have proposed here for the Rhodniini suggeststhat, at least for several lineages within the tribe, naturalselection of variants adapted to relatively dry microclimatesmay be related with the progressing of some species (andnot others) along the gradient of synanthropic behaviour.

Thus, all the populations of Rhodnius spp. that suc-ceed in colonising artificial environments (mainly of R.prolixus, but also of R. neglectus, R. nasutus, R. stali,R. pallescens, and R. ecuadoriensis) derive from ances-tral populations that adapted to arid or semi-arid climateslong before human beings reached the Americas. Alsowithin the Amazon, domestication foci (particularly ofR. stali, but also of T. maculata or P. herreri) are lo-cated in the regions with lowest mean annual rainfall orlongest rain-free periods (cf. Sombroek 2001). This pat-tern may in fact be even more general, affecting otherhumid forest triatomines; for instance, T. dimidiatapopulations seem to colonise human dwellings only outof the moist forests of the Yucatán-Petén region (Dornet al. 2007). These observations suggest that species orpopulations of triatomines that evolved to breed in ex-tremely humid microenvironments (such as Amazonianrainforest palm tree crowns) may have only a limitedpotential to successfully colonise artificial environ-ments, perhaps as a consequence of low tolerance to-wards the slightly drier microclimate of human dwell-ings. A prediction of this hypothesis is that field-col-lected specimens from moist forest ecotopes would failto thrive towards the drier end of an artificial humiditygradient in the laboratory. If confirmed, this pattern wouldsignal a truly evolutionary component of the process ofinfestation and colonisation of human environments bytriatomines. It could help us to identify differential risk ar-eas by mapping widely available climate data, and perhaps,in the future, to determine the potential for domiciliationof vector species or populations on an individual basis.

CONCLUSIONS

The systematic, ecological, and behavioural patternsof any group of organisms are gradually whittled alongthe evolutionary history of the lineage, from the moreor less ancient event at the origin of the clade to thecontemporary phenomena that shape the genetic struc-turing of conspecific populations. One major conse-quence, as Dobzhansky (1973) observed, is that adopt-ing an evolutionary perspective greatly widens our un-derstanding of those patterns, opening new paths in thesearch for satisfactory (realistic) answers to old diffi-

cult questions – from infectious disease control and sur-veillance to the mechanisms involved in the generation,maintenance and loss of biological diversity.

Equipped with ever more sophisticated analyticaltools (morphometrics, molecular markers, environmen-tal data obtained by remote sensors onboard artificialsatellites, radiocarbon dating) we can face the challengeof adopting this evolutionary stance in our research onChagas disease vectors, particularly when the questionsrefer to clearly monophyletic clades. Our review (pro-visional and incomplete) of the origin and diversifica-tion of Amazonian triatomines suggests research avenuesthat unfold in many directions, from the adequate under-standing of the evolution of whole tribes over millionsof years to the (probably necessary, and so far widelyneglected) demarcation of the truly evolutionary and‘merely’ ecological processes involved in the synan-thropic behavioural gradient of the Triatominae.

REFERENCES

Abad-Franch F, Monteiro FA 2005. Molecular research and thecontrol of Chagas disease vectors. An Acad Bras Cienc 77:437-454.

Abad-Franch F, Monteiro FA, Patterson JS, Miles MA 2003.Phylogenetic relationships among members of the PacificRhodnius lineage (Hemiptera: Reduviidae: Triatominae).Infect Genet Evol 2: 244-245.

Abad-Franch F, Palomeque FS, Aguilar VHM, Miles MA 2005.Field ecology of sylvatic Rhodnius populations (Heteroptera,Triatominae): risk factors for palm tree infestation in west-ern Ecuador. Trop Med Intl Health 10: 1258-1266.

Abad-Franch F, Paucar CA, Carpio CC, Cuba Cuba CA, AguilarVHM, Miles MA 2001. Biogeography of Triatominae (Hemi-ptera: Reduviidae) in Ecuador: implications for the design ofcontrol strategies. Mem Inst Oswaldo Cruz 96: 611-620.

Aguilar HM, Abad-Franch F, Dias JCP, Coura JR 2007. Chagasdisease in the Amazon region. Mem Inst Oswaldo Cruz(this volume).

Bargues MD, Marcilla JA, Ramsey J, Dujardin JP, Schofield CJ,Mas-Coma S 2000. Nuclear rDNA-based molecular clockof the evolution of Triatominae (Hemiptera: Reduviidae),vectors of Chagas disease. Mem Inst Oswaldo Cruz 95:567-573.

Barrett TV 1991. Advances in triatomine bug ecology in relationto Chagas disease. Adv Dis Vect Res 8: 143-176.

Brower AVZ 1994. Rapid morphological radiation and conver-gence in the butterfly, Heliconius erato, inferred from pat-terns of mitochondrial DNA evolution. Proc Nat Acad SciUSA 91: 6491-6495.

Carcavallo RU, Galíndez Girón I, Jurberg J, Lent H 1999. Atlasof Chagas Disease Vectors in the Americas, Vol. III,Fiocruz, Rio de Janeiro.

Cox CB, Moore PD 2000. Biogeography. An Ecological andEvolutionary Approach, Blackwell Science, Oxford.

Cuba Cuba CA, Abad-Franch F, Roldán RJ, Vargas VF, PollackVL, Miles MA 2002. The triatomines of Northern Peru, withemphasis on the ecology and infection by trypanosomes ofRhodnius ecuadoriensis (Triatominae). Mem Inst OswaldoCruz 97: 175-183.


de Paula AS, Diotaiuti L, Schofield CJ 2005. Testing the sister-group relationship of the Rhodniini and Triatomini (Insecta:Hemiptera: Reduviidae: Triatominae). Mol Phylogenet Evol35: 712-718.

de Paula AS, Diotaiuti L, Galvão C 2007. Systematics and bioge-ography of Rhodniini (Heteroptera: Reduviidae: Triatominae)based on 16S mitochondrial rDNA sequences J Biogeogr34: 699-712.

dos Santos CL, Lopes CM, Dujardin JP, Panzera F, Pérez R,Carbajal de la Fuente AL, Pacheco RS, Noireau F 2007.Evolutionary relationships based on genetic and phenetic char-acters between Triatoma maculata, Triatoma pseudomaculataand morphologically related species (Reduviidae: Triatominae).Infect Genet Evol doi:10.1016/j.meegid.2007.01.008.

Dobzhansky T 1973. Nothing in biology makes sense except inthe light of evolution. Am Biol Teacher 35: 125-129.

Dorn PL, Monroy C, Curtis A 2007. Triatoma dimidiata (Latreille,1811): A review of its diversity across its geographic rangeand the relationship among populations. Infect Genet Evol7: 343-352.

Galvão C, Carcavallo R, Rocha DS, Jurberg J 2003. A checklistof the current valid species of the subfamily TriatominaeJeannel, 1919 (Hemiptera, Reduviidae) and their geographi-cal distribution, with nomenclatural and taxonomic notes.Zootaxa 202: 1-36.

Gaunt MW, Miles MA 2002. An insect molecular clock dates theorigin of the insects and accords with palaeontological andbiogeographic landmarks. Mol Biol Evol 19: 748-761.

Gorla D 2002. Variables ambientales registradas por sensoresremotos como indicadores de la distribución geográfica deTriatoma infestans (Heteroptera: Reduviidae). Ecol Aus-tral 12: 117-127.

Hoorn C 1994. An environmental reconstruction of the pala-eo-Amazon river system (middle-late Miocene, NWamazonia). Palaeo 112: 187-238.

Hypša V, Tietz DF, Zrzavý J, Rego ROM, Galvão C, Jurberg J2002. Phylogeny and biogeography of Triatominae (Hemi-ptera: Reduviidae): molecular evidence of a New World ori-gin of the Asiatic clade. Mol Phylogenet Evol 23: 447-457.

Lent H, Wygodzinsky P 1979. Revision of the Triatominae (Hemi-ptera: Reduviidae), and their significance as vectors of Chagasdisease. Bull Am Mus Natural History 163: 123-520.

Marcilla A, Bargues MD, Abad-Franch F, Panzera F, CarcavalloRU, Noireau F, Galvão C, Jurberg J, Miles MA, Dujardin JP,Mas-Coma S 2002. Nuclear rDNA ITS-2 sequences revealpolyphyly of Panstrongylus species (Hemiptera: Reduviidae:Triatominae), vectors of Trypanosoma cruzi. Infect GenetEvol 1: 225-235.

Marcilla A, Bargues MD, Ramsey JM, Magallón-Gastélum E,Salazar-Schettino PM, Abad-Franch F, Dujardin JP, SchofieldCJ, Mas-Coma S 2001. The ITS-2 of the nuclear rDNA as a

molecular marker for populations, species, and phylogeneticrelationships in Triatominae (Hemiptera: Reduviidae), vec-tors of Chagas disease. Mol Phylogenet Evol 18: 136-142.

Matías A, de la Riva J, Martínez E, Torrez M, Dujardin JP 2003.Domiciliation process of Rhodnius stali (Hemiptera: Redu-viidae) in Alto Beni, La Paz, Bolivia. Trop Med Intl Health8: 264-268.

Miller SE 2007. DNA barcoding and the renaissance of taxono-my. Proc Natl Acad Sci USA 104: 4775-4776.

Mittermeier RA, Mittermeier CG, Brooks TM, Pilgrim JD,Konstant WR, da Fonseca GAB, Kormos C 2003. Wilder-ness and biodiversity conservation. Proc Natl Acad Sci USA100: 10309-10313.

Monteiro FA, Barrett TV, Fitzpatrick S, Cordón-Rosales C,Feliciangeli MD, Beard CB 2003. Molecular phylogeographyof the Amazonian Chagas disease vectors Rhodnius prolixusand R. robustus. Mol Ecol 12: 997-1006.

Monteiro FA, Lazoski C, Noireau F, Solé-Cava AM 2002.Allozyme relationships among ten species of Rhodniini, show-ing paraphyly of Rhodnius including Psammolestes. Med VetEntomol 16: 83-90.

Monteiro FA, Wesson DM, Dotson EM, Schofield CJ, Beard CB2000. Phylogeny and molecular taxonomy of the Rhodniiniderived from mitochondrial and nuclear DNA sequences. AmJ Trop Med Hyg 62: 460-465.

Morrone JJ 2006. Biogeographic areas and transition zones ofLatin America and the Caribbean islands based onpanbiogeographic and cladistic analyses of the entomofauna.Annu Rev Entomol 51: 467-494.

Olson DM, Dinerstein E, Wikramanayake ED, Burgess ND,Powell GVN, Underwood EC, D’Amico JA, Itoua I, StrandHE, Morrison JC, Loucks CJ, Allnutt TF, Ricketts TH, KuraY, Lamoreux JF, Wettengel WW, Hedao P, Kassem KR 2001.Terrestrial ecoregions of the World: a new map of life onEarth. Bioscience 51: 933-938.

Pavan MG, Monteiro FA 2007. A multiplex PCR assay that sepa-rates Rhodnius prolixus from members of the Rhodniusrobustus cryptic species complex (Hemiptera: Reduviidae).Trop Med Int Health 12: 751-758.

Rossetti DF, de Toledo PM, Góes AM 2005. New geologicalframework for Western Amazonia (Brazil) and implicationsfor biogeography and evolution. Quaternary Res 63: 78-89.

Schofield CJ, Dujardin JP 1999. Theories on the evolution ofRhodnius. Actual Biol (Medellín) 21: 183-197.

Sombroek W 2001. Spatial and temporal patterns of Amazon rain-fall. Consequences for the planning of agricultural occupationand the protection of primary forests. Ambio 30: 388-396.

WWF-World Wildlife Fund 2001. Ecoregions of Latin America andthe Caribbean. Available at http://www.conserveonline.org/docs/2001/06/lac_ecoregions.jpg

abdad franch & monteiro.2007.biogeography and evolution of amazonian mines

Documents