los ecotopos y la evolución de los triatominos y sus tryapanosomátidos asociados

7/27/2019 los ecotopos y la evolucin de los triatominos y sus tryapanosomtidos asociados

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558558558558558 Evolution of Triatomine Bugs and Trypanosomes M Gaunt, M Miles

Fig. 1: many triatomine species are adapted to specialist niches (see text). Top:Microtriatoma trinidadensis and its habitat, theleaves of aDidelphis nest. Centre:Eratyrus mucronatusand hollow tree inhabited by porcupines and arachnids. Bottom:Belminusherreri (left) and Panstrongylus lignarius (right) with its bark-like camoflauge colouration.


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559559559559559Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 95(4), Jul./Aug. 2000

large forest trees where it is associated with thelizard Thecadactylus; it appears to be an obligatelizard feeder. Panstrongylus lignarius adults movefreely over the surface of Amazonian trees and willapproach disturbances in the forest: their colora-

tion corresponds beautifully with the bark on whichthey reside, whilst younger stages lacking the cam-ouflage, live in tree holes. Triatoma tibiamaculata(in the State of Bahia, Brazil) lives in bromeliadepiphytes with pinkish camouflage that ideally suitsits habitat at the junction between the epiphyte andthe host tree. The peridomestic species T.rubrofasciata is almost invariably associated withthe ships rat (Rattus rattus) and is fortunately re-luctant to feed on most other hosts including hu-mans. Some triatomine species, however, such as

Rhodnius prolixus and P. megistus are obviouslyeclectic in their feeding, without obligate hosts.Nevertheless, the examples above suggest that ad-aptation of triatomine species to specialist nichesis commonplace, not exceptional.

The obscure spatial, feeding or temporal char-acteristics of some triatomine niches may reflect alack of information. One example is the difficultyin defining distinct niches for R. pictipes and R.robustus, both of which may be found in the samepalm tree. Yet, R. pictipes appears to be morecommonly associated with the mucaj palm

(Acrocomia sclerocarpa) andR. robustus with theinaj (Maximiliania regia) or the closely relatedbabau Orbigyna speciosa (Miles et al. 1983).These palm species prefer different soil types andhave different, albeit partially overlapping geo-graphical distributions. We suspect that the darkercolour ofR. pictipes and pinker light brown hue ofR.robustus may be indicative of their differentpalm tree habitats. Certainly, the coloration ofR.pictipes blends perfectly with the dry bases ofAcrocomia palm fronds. Distinct feeding nichesmight also be provided by subtle host preferences,for example,R.robustus has been tentatively as-sociated with the marsupial Caluromys philander(Caluromyidae). The greater ease with whichR.robustus adapts to laboratory colonies, com-pared toR.pictipes, may also reflect subtle micro-habitat differences. Finally present geographicaldistribution may in part be due to the contractionand expansion of forest relicts with climatic change.

The specialist adaptation of triatomine speciesto distinct niches implies a long evolutionary his-tory, as well as the dramatic more recent expan-

sion of a few eclectic, domiciliated species.HABITAT TRENDS OFRHODNIUS,PANSTRONGYLUS

AND TRIATOMA

Virtually all Rhodnius species are primarilyassociated with palm tree habitats (Lent &

Wygodzinsky 1979, Miles 1979, Carcavallo et al.1998). Exceptions areR. domesticus, reported frombromeliads and hollow trees, and R. paraensis,which has only been found once, in a tree hole ref-uge of the arboreal spiny ratEhimys chrysurus. As

mentioned, someRhodnius species may be asso-ciated with particular types of palm, further ex-amples beingR. brethesi with the palmLeopoldiniapiassaba andR. ecuadoriensis with Phytelephas.In addition to coloration (see above) other featuresofRhodnius may be adapted to life in palms, forexample, the climbing organs might assist move-ment along frond stems and trunks, which are par-ticularly smooth in many palm species. It followsthe distribution of sylvatic Rhodnius in LatinAmerica broadly coincides with the distribution of

palm trees. It is also not surprising that many spe-cies ofRhodnius will feed avidly on birds, whichcommonly nest in palms, especially on the fringesof forests and in open woodland. The genusPsammolestes, which is closely related toRhodniuscan be found in palms but especially in the nests ofAnumbius and Phacellodomus birds.

We believe therefore that the triatomine genusRhodnius, has a history of evolution in the palmtree habitat in Latin America.

Although some Panstrongylus species, such asP.megistus, can be found in palm crowns, all spe-

cies are predominantly associated with terrestrialburrows, tree root cavities and/or arboreal treeholes. A sylvatic habitat of the highly domicili-ated species P.megistus is arboreal tree holes withDidelphis (Miles et al. 1982). We suggest that thegenus Panstrongylus is primarily associated withburrows and tree cavities.

A survey of the habitat associations of speciesof the genus Triatoma (Miles 1979) reveals that atleast twenty Triatoma species are associated withterrestrial rocky habitats or rodent burrows. Anexception is T. sordida, which like Psammolestesseems to feed preferentially on birds. We suggestthat the genus Triatoma has evolved predominantlyin terrestrial, rocky habitats. The generaPanstrongylus and Triatoma are considered to beclosely related (tribe Triatomini) but more distantfromRhodnius (tribe Rhodniini).

These links between the three triatomine gen-era and habitat type are summarised in Table I.Although not absolute, these associations are re-markable in view of the many opportunities thatmust have arisen for the colonisation of alterna-

tive niches.Indeed the substrate preferences ofRhodnius,

Panstrongylus and Triatoma are reflected in theirdistribution within infested houses. Thus, R.prolixus can give heavy infestations in palm roofs;P. megistus is primarily associated with earth and


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wooden substrates of timber framed, mud walledhouses but seldom colonises palm roofs, and T.infestans can be found in good quality housing andin tiled roofs.

HABITAT AND HOST ASSOCIATIONS OF T.CRUZI1

(Z1), T.CRUZI2 (Z2) AND Z3

T.cruzi Z1 and T. cruzi Z2 were originally de-scribed on the basis of isoenzyme phenotypes asmajor subdivisions within the species T. cruzi.They were more widely separated by isoenzymecriteria than unequivocal biologically distinct spe-cies of the genusLeishmania (Miles et al. 1983).Z3 was described as a group without certain af-finities to Z1 or Z2. Over the last two decades aplethora of molecular methods including randomamplification of polymorphic DNA (RAPD), de-

termination of ribosomal and mini-exon DNA se-quence polymorphisms, and microsatellite analy-sis have confirmed the integrity of two major sub-divisions within T.cruzi, corresponding to Z1 andZ2. A recent workshop (Anon 1999) attempted toconsolidate various terminologies (and to removeconfusion that arose when Z1 and Z2 were namedon ribosomal DNA sequence data as lineage 2 andlineage 1 respectively) by naming the two subdi-visions as T. cruzi 1 (Z1) and T. cruzi 2 (Z2). Thereis marked heterogeneity also within T.cruzi 1 and

T.cruzi 2, particularly within the latter. Tibayrencand his collaborators have studied this heteroge-neity in great detail (Bastrenta et al. 1999). SomeT.cruzi strains appear to have characteristics typi-cal of both T.cruzi 1 and T.cruzi 2, suggesting theoccurrence of genetic recombination and hybridforms (Stothard et al. 1999). Although T.cruzi ap-pears to be predominantly clonally propagated,field and experimental evidence implies a capac-ity for genetic exchange, at least in T.cruzi 1(Stothard et al. 1999). A few T.cruzi isolates fromthe Amazon basin appear to share T.cruzi 1 (Z1)

and Z3 characters (Povoa et al. 1984). More de-

tailed molecular studies suggest Z3 has closest af-finities with T.cruzi 2 (Z2).

A large number of T.cruzi isolates from theAmazon basin have been identified as T.cruzi 1(Z1) or Z3, although this work is far from compre-

hensive as not all mammal or triatomine speciesare well represented in these surveys (Povoa et al.1984). Nevertheless, T.cruzi 1 (Z1) was consis-tently isolated from the common opossum (D.marsupialis) and was also found inR.robustus andR.pictipes (Povoa et al. 1984, Carrasco et al. 1996).This accords with the frequent isolation ofT.cruzi1 (Z1) fromDidelphis elsewhere. We concludedthat there is a close but not absolute associationbetween palm trees,Rhodnius species, T.cruzi 1(Z1) andDidelphis (Table I).

The T.cruzi subgroup Z3, with as yet unre-solved affinities, was associated in the Amazonbasin with an edentate, the armadillo Dasypusnovemcinctus, and with the terrestrial marsupialMonodelphis brevicaudata (Povoa et al. 1984). Z3was also isolated from P.geniculatus, the triatominebug commonly found in armadillo burrows. Weconcluded that Z3 may be primarily associated withthe terrestrial habitat and ground dwelling hosts(Povoa et al. 1984, Table I).

T.cruzi 2 (Z2) predominates in domestic trans-mission cycles in the southern cone countries of

South America [Argentina, Bolivia, Brazil, Chile,Paraguay and (presumably) Uruguay] (Miles et al.1984, Chapman et al. 1984), whereas T.cruzi 1(Z1) predominates in domestic transmission cyclesto the north of the Amazon basin. T. infestans isthought to have spread from a sylvatic habitat inBolivia among rocks inhabited by guinea pigs(Cavia) throughout the entire region of domesticT.cruzi transmission in the southern cone coun-tries. This led us to suggest that there is a strongassociation between T.cruzi 2 (Z2), Triatoma androdents, and the terrestrial habitat (Table I). Im-portantly, T.cruzi 2 (Z2) has also been linked to

TABLE I

Triatomine habitats, hosts and trypanosomes

Triatomine Silvatic Ecotope Associated Trypanosomes Associated Hosts

Rhodnius species Arboreal: palms Trypanosoma cruzi 1 [Z1] Marsupial (Didelphis)T. rangeli Marsupial (Didelphis)

Panstrongylus Arboreal: not palms T. cruzi 1 [Z1] Didelphis

Panstrongylus Terrestrial: burrows T. cruzi [Z3] EdentateDasypus

MarsupialMonodelphis

Triatoma Terrestrial: rocks T. cruzi 2 [Z2] [Edentates?]a

Rodents (Cavia)Primates (Leontocebus)

a: edentates proposed as original hosts, see Table II and text.


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primates in southern Brazil (Leon tocebus)(Fernandes et al. 1999).

Not surprisingly there are exceptions to thesegeneral associations, for example, T.cruzi 1 (Z1)has been isolated from T. spinolai in Chile (Miles

et al. 1984) and T.cruzi 1 (Z1) has been isolatedfrom P.geniculatus infesting pigsties in the Ama-zon basin (Valente et al. 1998).

THE EVOLUTION OF T.CRUZI1 (Z1), T.CRUZI2 (Z2)

AND Z3

The observations above suggest a link betweenT.cruzi 1 (Z1) andDidelphis, and between T.cruzi2 (Z2) and rodents or primates. The early mam-

mal inhabitants of South America were the marsu-pials, and the placental edentate mammals (arma-dillos, sloths and anteaters) around 65 million yearsago. However, fossil evidence indicates that ro-dents, primates and bats arrived about 25 million

years later (Fig. 2). Furthermore rodents and pri-mates probably reached South America from Af-rica, whereas marsupials and edentates migratedsouthwards from North America. Molecular evi-dence suggests that T.cruzi 1 (Z1) and T.cruzi 2(Z2) diverged between 88 and 37 million years ago,although this requires confirmation with other datasets (Briones et al. 1999). IfT.cruzi 2 (Z2) is in-

Million

years ago

South American

land mammal ages

First appearances in south America

PLEISTOCENE

PLIOCENE

Cricetidae, Mustelidae, Felidae, Canidae

Ursidae, Camelidae, Cervidae, Tayassuidae

Gomphotheriidae, Equidae, Tapridae

Leporidae, Soricidae, Sciuridae

MIOCENE Procyonidae

OLIGOCENE

EOCENE Primates

Caviomorpha

PALEOCENE

CRETACEOUS

Marsupalia, Xenartha, Condylarthra

Litopterna, Notoungulata, Astrapotheria

Trigonostylopoidea, Pyrotheria, Xenungulata

0

5

10

15

20

25

30

35

40

45

50

55

60

65

Fig. 2: marsupials and edentates are thought to have been present in South America 65 million years ago and 25 million yearsbefore the arrival of primates and rodents (based on Webb & Marshall 1982).


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deed primarily associated with rodents or primatesthis implies a more recent evolutionary history thanthat ofT.cruzi 1 (Z1).

Based on the observations described here wepropose the following for the evolutionary histories

ofT. cruzi 1 (Z1), T.cruzi2 (Z2) and Z3: (i) T.cruzi1 (Z1) has evolved in an arboreal, palm tree habitat,with the triatomine tribe Rhodniini and also in asso-ciation with the opossumDidelphis; (ii) both T.cruzi2 (Z2) and Z3 evolved in a terrestrial habitat in bur-rows and in rocky locations, with the triatomine tribeTriatomini, in association with ground dwellingedentates, and possibly ground dwelling marsupi-als. Thus, edentates could be the primary host ofboth T.cruzi 2 (Z2) and Z3 and both the major sub-divisions ofT.cruzi could have been contemporary

in South America up to 65 million years ago, andboth have evolved in South America. If this hy-pothesis is correct, it follows that T.cruzi 2 (Z2) hasreached rodents in later times through the sharedterrestrial ecotope with edentates, and primateswould also represent secondary hosts. We wouldexpect that additional molecular evidence will con-firm that Z3 is more closely related to T.cruzi 2 (Z2)than to T.cruzi 1 (Z1). An alternative hypothesis isthat there was no early association between T.cruzi2 (Z2) and edentates and that all T.cruzi2 (Z2) popu-lations are more recently derived from T.cruzi 1

(Z1) by host transfer into rodents, edentates and pri-mates (Table II). Molecular dating evidence willbe crucial (see below) to determining whether thereis an ancient association between T. cruzi 2 (Z2)and edentates.

T.rangeli isDidelphis, and geographical distribu-tion ofT.rangeli broadly corresponds with that ofRhodnius species and Didelphis. We thereforeassume that like T. cruzi 1 (Z1), T.rangeli hasevolved in an arboreal palm tree habitat with the

Rhodniini and withDidelphis. Molecular evidenceindicates that there is heterogeneity within the spe-cies T.rangeli. Further clarification of the rela-tionship between T.rangeli and T.cruzi may de-pend on molecular phylogenetic studies.

The relatively recent arrival of bats to SouthAmerica and their mobility by flight, suggests thatT.cruzi like trypanosomes of bats are derived fromeither T.cruzi 1 (Z1) or T.cruzi 2 (Z2)/Z3 by habi-tat sharing or, for insectivorous bats, by consump-tion of infected triatomine bugs. Several bat genera

are common to South America and to the Old World.Molecular phylogenetic studies should revealwhether bat trypanosomes are closely related to oneor both of the T.cruzi subdivisions and whetherT.cruzi does indeed pre-date bat Schizotrypanum.

T. conorhini is unusual in that it is specificallyassociated withR. rattus and rubrofasciata, whichmay have spread from North America to the OldWorld. IfT.conorhini also has a New World ori-gin and affinities with T.cruzi we might expectmolecular evidence to show that it is more closelyrelated to T.cruzi 2 (Z2) than T.cruzi 1 (Z1).

THE LINK WITH AUSTRALIA

Stevens et al. (1999) have suggested an evolu-tionary link between a trypanosome of Australianmarsupials (kangaroo) and T.cruzi. Australianmarsupials are likely to be derived from one or afew species of the South American fauna whichreached Australia via Antarctica around 45 mil-lion years ago. If we assume that the Triatominaeevolved in South America (with the possible ex-ception of the aberrant Indian genusLinshcosteus)it is perhaps not surprising that triatomine bugs did

not reach Australia. Whilst of no proven evolu-tionary significance, it is interesting to note thatMiles et al. (1982) commented on the kangaroo-like terrestrial locomotion of the marsupialMetachirus nudicaudatus in Brazilian forest.

THE EVOLUTION OF TRIATOMINE BUGS

The occurrence of infective (metacyclic) T.cruziin anal glands of the opossumDidelphis has sug-gested that T.cruzi might have been transmitted di-rectly from marsupial to marsupial without atriatomine vector. In this case, triatomine bugswould have acquired T.cruzi infections only afterT.cruzi had evolved as a blood parasite of marsupi-als. The alternative view is that T.cruzi has arisenfrom a flagellate parasite or symbiont of insects.Many flagellates, including kinetoplastids, are found

TABLE II

Proposed habitat and host associations for the twomajor subdivisions ofTrypanosoma cruzi

(T. cruzi 1 and 2)

T. cruzi 1 Z1 has evolved withDidelphis and

(Marsupial) Rhodnius in an arboreal ecotope(palms)

T. cruzi 2 Z2 have both evolved initially with(Edentate) Z3 edentates and Triatoma/Pans-

trongylus in a terrestrial ecotope

T. cruzi 2 Z2 has reached rodents through theshared terrestrial ecotope withedentates

T. RANGELI, BAT SCHIZOTRYPANUM AND T.

CONORHINI

T. rangeli is virtually exclusively associatedwith the triatomine tribe Rhodniini and the genusRhodnius, in which T.rangeli can reach the sali-vary glands to be transmitted by the bite, and notby faecal contamination. A common host of


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in insects, and do not have a vertebrate host. Onceagain, molecular phylogenetics is likely to be fun-damental to resolving this question.

Schofield (this volume) has quite logically sug-gested that the haematophagous triatomine bugs

arose from predatory reduvids in response to theavailability of vertebrate as well as invertebratefood sources in animal refuges and nesting sites.It is possible that the transition from predation tohaematophagy may have occurred on more thanone occasion. Several reduvid predators aremorphologicaly similar to triatomines. However,the transition to haematophagy may not have beenstraightforward in that it presumably demands theevolution of anti-thrombins, to prevent coagula-tion interfering with feeding, and of less painful

bites to allow prolonged feeding.As marsupials and edentates were extant inSouth America at least 65 million years ago andwere presumably using similar abundant arborealand terrestrial nesting sites, we have no reason tobelieve that the triatomine transition tohaematophagy did not take place long ago, andperhaps at a similar time, that is late in the Creta-ceous or early in the Cenozoic (Paleocene, Eocene).It is significant to this debate to determine the evo-lutionary age of triatomine bugs. Accordingly wehave begun to apply an extensive molecular

phylogenetics approach to elucidate the evolutionand ecology of triatomines using both mitochon-drial DNA and nuclear targets.

VECTOR PHYLOGENETICS

The phylogenetic analysis of DNA sequencedata has proved a powerful method for addressingboth macro- and micro-evolutionary hypotheses forthe origins, epidemiological structure and popula-tion dynamics of both arthropod vectors and theirspecific parasites (Garcia & Powell 1998, Stothardet al. 1998, Lyman et al. 1999, Stevens & Gibson

1999, Stevens et al. 1999). The questions raisedso far fall into the macro-evolutionary category,however questions of evolution in micro-timescales are receiving increasing attention in the fielddue to their usefulness in determining the popula-tion dynamics of triatomine bugs (Harry et al.1998).

Our investigation of the epidemiology ofChagas disease from the perspective of vector evo-lution has two approaches: firstly, as a study ofmacro-evolution, that is the molecular reconstruc-

tion of the vector in relation to other insect vec-tors, as well as estimating the evolutionary time-scale involved, and secondly as a study of the mi-cro-evolution of triatomine bug population dynam-ics. Triatomine molecular approaches are topicallargely because of the successful control of Chagas

disease transmission by the eradication of domes-tic T. infestans in the recent southern coneprogramme (Dias & Schofield 1999). Our initialanalysis describes the evolution of the triatomineswith respect to the other major haematophagous

vectors through a mitochondrial DNA phylogenycomprisingAedes, Culex andAnopheles mosqui-toes, biting midges, black flies, and tsetse. To ourknowledge this represents the largest phylogenyof haematophagous vectors between genera. Thephylogeny is divided into two clades one contain-ing the homometabolous insects and the other thehemimetabolous insects. The evolution of diseasetransmission is a question that can be addressedby phylogeny, that is the evolution of faecal trans-mission (cophageny) of vector-borne diseases in

comparison to that of salivary transmitted parasites.Triatomines are anomalous as an arthropod vectoras they transmit trypanosomes both through con-taminated faeces (T. cruzi) and salivary transmis-sion (T. rangeli). A comparative analysis of thefive vectors phylogeny with the inclusion of otherinsects, particularly termites, harboring protozoanendosymbionts provides several lines of evidencethat faecal transmission is ancestral. In addition,triatomines demonstrate exclusive cophageny forbacterial symbionts (Durvasula et al. 1999), andpredominant cophageny for the triatomine patho-

genBlastocrithidia triatomae (Schaub et al. 1989).The evidence suggests that the original bug-bornetrypanosome hijacked the natural mechanism ofendosymbiont transmission.

A second focus of our macro-evolutionary stud-ies has concerned evolutionary dating. The datingof insects remains problematic due to the relativescarcity of their fossil record (Ross & Briggs 1993)and the surprising absence of molecular clocks evenat the family level. Following an extensive searchwe obtained a single genetic locus demonstratingclock behaviour both between lineages (constantrates of evolution) and between nodes (the con-gruence of the fossil record) for all available se-quence data within the classInsecta. The molecu-lar clock phylogeny describes the deepest splitwithin the triatomines betweenRhodnius and Tri-atoma as being ancient, occurring before the ar-rival of bats and rodents into South America. Com-bined with the niche specialization of triatominesa unified picture of an ancient family emerges. Themolecular clock has much broader implications forother insect groups, although our chief concern is

the ability to obtain robust dates for the speciesdivergences within the Triatominae. This wouldelucidate the time-scale for the evolution of theniche specialization previously described, andwould include the time for the evolution of bugsinto domestic habitats.


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The evolutionary understanding of thetriatomines is furthered by our recent observationof the monophyletic origin of anti-thrombin sali-vary proteins within the triatomine family and pro-vides compelling evidence that the evolution of

haematophagous behaviour evolved from a singleancestor. A large focus of research interest con-cerns the phylogenetic status of predatory reduvi-ids, some of which have been postulated to splitthe monophyly of the triatomines. Such an occur-rence would be of particular evolutionary interestfor haematophagous vectors.

The focus of our micro-evolutionary studiesconcerns the movement of bugs between sylvaticand domestic ectopes. To address this issue wedeveloped a salivary protein phylogeny based on

anti-thrombin proteins for all the major species inthe genusRhodnius, and we are currently devel-oping further salivary protein genetic markers. Thecurrent phylogeny was congruent with the corre-sponding mitochondrial phylogenies already de-scribed by Lyman et al. (1999), with the singleexception, ofR. neglectus which for salivary pro-tein phylogenies forms a sister group with R.nasutus. The salivary protein genetic marker pro-vides high genetic resolution for the genusRhodnius, resulting in robust bootstrap support foreven closely relatedR.prolixus populations cap-

tured in Nicaragua and Honduras. Moreover, theability to distinguish betweenR.prolixus popula-tions from adjacent countries appears to provide aconsiderable advantage over the starch gel elec-trophoresis of salivary haeme proteins, which wereunable to distinguish Honduras R. prolixus fromVenezuelan populations (Sores et al. 1998).

The aim of both our evolutionary approachesis to adapt evolutionary dating into a micro-evolu-tionary time scale using the high resolution sali-vary protein genetic markers. The strategy wouldpotentially determine the age of the split betweentriatomines that have evolved within an exclusivelysylvatic ecotope and those that have irreversiblyadapted to a domestic ectope e.g. T. infestans.Robust estimates of micro-evolutionary time be-tween or within species complexes represents im-portant information for assessing the feasibility ofvector eradication by insecticide programmes andsuccess would be a seminal contribution to resolv-ing haematophagous vector population dynamics.

Ultimately it is the combination of both vectorand parasite phylogenies as well as the interface

between macro-evolution and micro-evolution thatforms part of a cross-disciplinary approach forunderstanding Chagas disease epidemiology. Thisin turn provides a comprehensive framework foradvising South American governments on cost ef-fective control strategies for Chagas disease

through the recently formed ECLAT network. Theresearch reviewed here is an integral componentof the ECLAT objectives.

ACKNOWLEDGEMENTS

To Chris Schofield, Jos Jurberg, Aldo Valente,Mariela Torres-Torres, Ben Beard, Cesar Cuba Cuba,Russell Stothard and Hooman Momen for supplying bugspecimens and/or for helpful discussions. To Susi Solisfor assistance as part of her ALFA training programme.

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los ecotopos y la evolución de los triatominos y sus tryapanosomátidos asociados

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