Systematics and biogeography of Rhodniini (Heteroptera ... · Ecuador and northern Peru and Rhodnius pallescens Barber, 1932 in Panama and parts of Colombia. Other Rhodnius species

ORIGINALARTICLE

Systematics and biogeography ofRhodniini (Heteroptera: Reduviidae:Triatominae) based on 16S mitochondrialrDNA sequences

Alexandre Silva de Paula1*, Lileia Diotaiuti1 and Cleber Galvao2

1Laboratorio de Triatomıneos e Epidemiologia

da Doenca de Chagas, Centro de Pesquisas

Rene Rachou/FIOCRUZ, Av. Augusto de Lima

1715, 30190-002 Belo Horizonte, MG and2Laboratorio Nacional e Internacional de

Referencia em Taxonomia de Triatomıneos,

Departamento de Protozoologia, Instituto

Oswaldo Cruz/FIOCRUZ, Av. Brasil 4365,

21040-900 Rio de Janeiro, RJ, Brazil

*Correspondence: Alexandre Silva de Paula,

Laboratorio de Triatomıneos e Epidemiologia

da Doenca de Chagas, Centro de Pesquisas Rene

Rachou/FIOCRUZ, Av. Augusto de Lima 1715,

30190-002 Belo Horizonte, MG, Brazil.

E-mail: [email protected]

ABSTRACT

Aim The tribe Rhodniini is one of six comprising the subfamily Triatominae

(Heteroptera: Reduviidae), notorious as blood-sucking household pests and

vectors of Trypanosoma cruzi throughout Latin America. The human and

economic cost of this disease in the American tropics is considerable, and these

bugs are unquestionably of great importance to man. Studies of the evolution,

phylogeny, biogeography, ecology, physiology and behaviour of the Rhodniini are

needed to help improve existing Chagas’ disease control programmes. The

objective of the study reported here was to propose biogeographical hypotheses to

explain the modern geographical distribution of the species of Rhodniini.

Location Neotropical region.

Methods We employed mitochondrial rDNA sequences (16S) currently

available in GenBank to align sequences of Rhodniini species using ClustalX.

The analyses included 16S sequences from predatory reduviid subfamilies

(Stenopodainae, Ectrichodiinae, Harpactorinae, Reduviinae and Salyavatinae)

present in GenBank as an outgroup. Cladistic analysis used the program PAUP to

derive trees based on maximum parsimony (MP) and maximum likelihood (ML).

Known distribution data for Rhodniini species were obtained from reviews and

plotted on maps of South and Central America using the program iMap. An area

cladogram was derived from the cladistic result to show the historical connections

among the studied taxa and the endemic areas. The program TreeMap (Jungle

Edition) was used to deduce taxon–area associations where the optimal solutions

to explain the biogeographical hypothesis of the Rhodniini in the Neotropics were

those with lowest total cost.

Results Parsimony and maximum-likelihood analysis of 16S rDNA sequences

included 14 species of Rhodniini, as well as five species of predatory Reduviidae

representing five of the predatory subfamilies. Tanglegrams were used to show the

relationship between the Neotropical areas of endemism and Rhodniini species.

When TreeMap with codivergence (vicariance) events were weighted as 0 and

duplication (sympatry), lineage losses (extinction) and host switching (dispersal)

were all weighted as 1, 20 scenarios were found to explain the biogeographical

history of Rhodniini in the Neotropical region. Twelve of the optimal solutions

with the lowest total cost were used to explain the biogeography of the Rhodniini

in the Neotropics. These optimal reconstructions require six vicariance events, 20

duplications (sympatry), at least three dispersals, and at least one extinction

event.

Main conclusions The Rhodniini have a complex biogeographical history that

has involved vicariance, duplications (sympatry), dispersal and extinction events.

The main geological events affecting the origin and diversification of the

Rhodniini in the Neotropics were (1) uplift of the Central Andes in the Miocene

Journal of Biogeography (J. Biogeogr.) (2007) 34, 699–712

ª 2006 The Authors www.blackwellpublishing.com/jbi 699Journal compilation ª 2006 Blackwell Publishing Ltd doi:10.1111/j.1365-2699.2006.01628.x

INTRODUCTION

The tribe Rhodniini Pinto, 1926 is one of six comprising the

subfamily Triatominae (Heteroptera: Reduviidae), notorious

as blood-sucking household pests and vectors of Trypanosoma

cruzi Chagas, 1909 throughout the Neotropics (Galvao et al.,

2003). Their genera belong to a well defined monophyletic

group (Lent & Wygodzinsky, 1979). Morphological characters

can be used to distinguish Rhodnius Stal, 1859 and Psammo-

lestes Bergroth, 1911, the two genera of Rhodniini, particularly

the apically inserted antennae and the presence of distinct

callosities behind the eyes (Lent & Wygodzinsky, 1979).

Species of Rhodnius are primarily arboreal, often occupying

ecotopes in palm tree crowns or epiphytic bromeliads. The

genus is widely distributed in South and Central America. In

Central America and the northern Andean countries (Peru,

Ecuador, Colombia and Venezuela), Rhodnius species are

primary targets of Chagas’ disease vector control initiatives.

This is particularly true for Rhodnius prolixus Stal, 1872, as well

as Rhodnius ecuadoriensis Lent & Leon, 1958 in parts of

Ecuador and northern Peru and Rhodnius pallescens Barber,

1932 in Panama and parts of Colombia. Other Rhodnius

species have local epidemiological importance, including

Rhodnius neglectus Lent, 1954 and Rhodnius nasutus Stal,

1859 in central and northeastern Brazil; Rhodnius stali Lent

et al., 1993 in Bolivia; and Rhodnius brethesi Matta, 1919 in the

Brazilian Amazon (Schofield & Dujardin, 1999). The genus

Rhodnius was reviewed by Lent (1948), Lent & Jurberg (1969),

Lent & Wygodzinsky (1979). Three additional species have

since been described: R. stali (Lent et al., 1993), Rhodnius

colombiensis (Moreno et al., 1999) and Rhodnius milesi

(Valente et al., 2001). The genus Rhodnius currently has 16

recognized species, including Rhodnius dalessandroi Carcavallo

& Barreto, 1976 and Rhodnius paraensis Sherlock et al., 1977,

neither of which has been collected since its original descrip-

tion.

The genus Psammolestes includes Psammolestes arturi

(Pinto), 1926, Psammolestes coreodes Bergroth, 1911 and

Psammolestes tertius Lent & Jurberg, 1965 (Galvao et al.,

2003). The genus was reviewed by Lent & Jurberg (1965) and

Lent & Wygodzinsky (1979). Species of Psammolestes live in

birds’ nests. They do not associate with man, and only rarely

with other mammals; as such they are not important in

T. cruzi transmission (Lent & Wygodzinsky, 1979).

The importance of the Rhodniini lies in the fact that some of

its members feed on humans and many of these transmit

T. cruzi, the protozoan that causes Chagas’ disease. The human

and economic costs of this disease in the American tropics are

considerable (Schaefer, 2005).

A wide variety of reasons have been proposed for the high

biological diversity seen in the Neotropics (Amorim, in press).

Accepted causes of disjunction include: (1) tectonic displace-

ment, (2) sea-level fluctuations, (3) interspecific competition

together with climate change, (4) parapatric speciation along

environmental gradients, (5) pest pressure, and (6) fine-scale

habitat heterogeneity (for details see Amorim, 2006).

The first two of these causes are classed as palaeogeograph-

ical, being Mesozoic–Lower Tertiary events, while the latter

four occurred mainly in the Quaternary. Some of them

represent competing explanations for the same biological

events. Most of the causes proposed for species diversification

in these models were not inferred based on a given method of

biogeographical reconstruction, but rather were chosen a pri-

ori based on other sources of evidence (Amorim, in press).

Several Neotropical groups of organisms have species that

are widely distributed throughout South and Central America

(Amorim, in press). However, groups as divergent as mammals

and insects also contain species with restricted and overlapping

geographical distributions. The areas of endemism proposed

by dispersionists, refuge theory biogeographers and vicariance

biogeographers, based on studies of different groups such as

insects, arachnids, mammals and plants, are largely congruent.

Thus, despite disagreements about the causes of cladogeneses,

different biogeographical schools largely concur regarding the

boundaries of the main areas of endemism in the Neotropics

(Fig. 1). This strongly suggests common causes for the origin

of these patterns.

Methods that allow for both dispersal and vicariance have

been proposed to reconstruct biogeographical history

(Ronquist, 1997). Hence there is a growing plurality in the

theoretical and methodological tools of biogeography. Never-

theless, few empirical studies have documented the relative

roles of vicariance and dispersal (Zink et al., 2000). The aim of

the study reported here was to formulate biogeographical

or later, (2) break-up of the Andes into three separate cordilleras (Eastern,

Central and Western) in the Plio-Pleistocene, (3) formation of a land corridor

connecting South and North America in the Pliocene, and (4) uplift of the Serra

do Mar and Serra da Mantiqueira mountain systems between the Oligocene and

Pleistocene. The relationships and biogeographical history of the species of

Rhodniini in the Neotropical region probably arose from the areas of endemism

shown in our work.

Keywords

Chagas’ disease control, Hemiptera, historical biogeography, Neotropical,

Psammolestes, rDNA mitochondrial gene, Rhodnius, Triatominae.

A. S. Paula, L. Diotaiuti and C. Galvao

700 Journal of Biogeography 34, 699–712ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd

hypotheses to explain the modern geographical distribution of

Rhodniini species. Both systematic and biogeographical

approaches were used to construct testable hypotheses, using

area cladograms (Cracraft, 1994) and the program TreeMap

2.02 (Charleston & Page, 2001). The biogeographical hypoth-

esis was formulated using Amorim’s (in press) historical

reconstruction of the Neotropical region (Fig. 2).

METHODS

Systematics

In the present study we used mitochondrial rDNA sequences

(16S) currently available in the NCBI genetic database. Other

genes currently available in the NCBI database (e.g. 12S,

cytochrome oxidase 1, cytochrome b, and nuclear rDNA

sequences 18S and ITS2) were not considered because of the

methodological difficulties of combining sequence information

from different genes (Kitching et al., 1998; Sanderson &

Shaffer, 2002), and the fact that different genes were

represented by unequal taxon sets in the construction of the

outgroup. Initial analyses were made by aligning groups of

sequences using ClustalX 1.83 (Thompson et al., 1997) under

gap-opening/gap-extension penalties 15/9, 15/6, 15/3, 9/6, 9/3,

6/3, and by treating the gaps as missing (?). The analyses

included the available 16S sequences from predatory reduviid

subfamilies present in GenBank as an outgroup: Stenopoda

spinulosa Giacchi, 1969 (Stenopodainae); Ectrychotes andreae

(Thunberg), 1784 (Ectrichodiinae); Sycanus croceus Hsiao,

1979 (Harpactorinae); Tiarodes venenatus Matsumura, 1913

(Reduviinae); Lisarda rhypara Stal, 1858 (Salyavatinae)

(Table 1). The outgroup was chosen based on the findings of

Paula et al. (2005) and the fact that the ancestral form of

Rhodnius was placed in the Stenopodainae by Schofield &

Dujardin (1999).

The species R. dalessandroi, R. paraensis, Rhodnius amazo-

nicus, R. milesi and P. arturi were not included in this analysis

because there were no gene sequences for them in GenBank.

Cladistic analysis used the program PAUP 4.0b10 (Swofford,

2002) to derive trees based on maximum parsimony (MP) and

Figure 1 Simplified picture of main areas of

endemism for Neotropical organisms based

on vertebrates, insects and other groups. The

mere existence and the limits of areas of

endemism are always hypotheses that may be

corrected with additional studies. Although

there may be additional areas, there are

insufficient data to attain a minimally reliable

hypothesis. (Source: artwork provided by Dr

Dalton de Souza Amorim – Faculdade de

Filosofia, Ciencias e Letras de Ribeirao Preto/

USP; see Amorim & Pires, 1996).

Systematics and biogeography of Rhodniini

Journal of Biogeography 34, 699–712 701ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd

maximum likelihood (ML). Parsimony branch-and-bound

searches were performed on the alignments using the chosen

outgroup. Characters were treated as unordered and of equal

weight, and the trees were rooted at an internal node with basal

polytomy. Strict consensus trees were then obtained for each

branch-and-bound search. Parsimony bootstrap analyses were

conducted employing a heuristic search with 100 bootstrap

replicates using 10 random stepwise addition (tree-bisection-

reconnection, TBR). Strict consensus trees were obtained from

all the retained trees in the branch-and-bound searches, and

Figure 2 General biogeographical pattern of

the Neotropical region based on different

groups of vertebrates, insects and plants. The

first vicariant event corresponds to the

separation of the Caribbean arc from the

continental Neotropical region. The second

event divides north-west South America,

Central America and coastal Mexico (NW)

from south-east South America (SE). The

third event separates Central America and the

Choco regions from the Amazonian forest in

the NW Neotropical component, and south-

east Amazonia from the Atlantic Forest in the

SE Neotropical component. (Source: artwork

provided by Dr Dalton de Souza Amorim –

Faculdade de Filosofia, Ciencias e Letras de

Ribeirao Preto/USP; Amorim, in press).

Table 1 Species and 16S ribosomal DNA

gene (mitochondrial gene) sequences used in

maximum parsimony and maximum likeli-

hood analyses

Taxa Accession no. Length %GC

Outgroup

Stenopodainae

Stenopoda spinulosa Giacchi, 1969 AY252684 314 28.0

Ectrichodiinae

Ectrychotes andreae (Thunberg, 1784) AY127035 508 27.0

Harpactorinae

Sycanus croceus Hsiao, 1979 AY127043 510 30.0

Reduviinae

Tiarodes venenatus Matsumura, 1913 AY127045 509 32.0

Salyavatinae

Lisarda rhypara Stal, 1858 AY127039 508 29.0

Ingroup

Rhodnius pallescens Barber, 1932 AF045706 374 24.0

Rhodnius ecuadoriensis Lent & Leon, 1958 AF028746 285 23.0

Rhodnius colombiensis Mejia, Galvao & Jurberg, 1999 AY035438 510 28.0

Rhodnius pictipes Stal, 1872 AF045709 373 26.0

Rhodnius stali Lent, Jurberg & Galvao, 1993 AY035437 508 29.0

Rhodnius prolixus Stal, 1859 AF045707 373 27.0

Rhodnius nasutus Stal, 1859 AF028749 284 24.0

Rhodnius neglectus Lent, 1954 AF045704 372 29.0

Rhodnius robustus Larrousse, 1927 AF045705 372 30.0

Rhodnius domesticus Neiva & Pinto, 1923 AY035440 508 32.0

Rhodnius brethesi Matta, 1919 AF045710 374 27.0

Rhodnius neivai Lent, 1953 AY035441 508 31.0

Psammolestes coreodes Bergroth, 1911 AF045708 371 27.0

Psammolestes tertius Lent & Jurberg, 1965 AY035439 503 30.0

Species of subfamilies Stenopodainae, Ectrichodiinae, Harpactorinae, Reduviinae and Salyava-

tinae were used as outgroups (see Methods). Length ¼ DNA sequence length; %GC ¼ guanine/

cytosine content.



the topology of each tree under individual gap-opening/gap-

extension penalties was tested with ML, using a model of

estimated gamma distribution (discrete approximation),

HKY85 variant to allow for transition/transversion bias,

unequal base frequencies and different substitution rates (Page

& Homes, 1998), empirical base frequencies and an estimated

substitution model following heuristic stepwise addition using

TBR branch-swapping.

Biogeography

Distributional data for Rhodnius species were obtained from

reviews by Lent (1948), Lent & Jurberg (1969), Lent

& Wygodzinsky (1979). Additional localities for R. stali,

R. colombiensis, R. milesi and R. amazonicus were obtained

from Lent et al. (1993), Moreno et al. (1999), Valente et al.

(2001) and Berenger & Pluot-Sigwalt (2002), respectively.

Distributional data for Psammolestes species were obtained

from Lent & Jurberg (1965) and Lent & Wygodzinsky (1979).

Coordinates of the localities were obtained from Vanzolini &

Papavero (1969) and Brown (1979). Species distributions were

plotted on maps of South and Central America using the

program iMap 3.1 for Apple Macintosh.

Phylogenetic analysis of Rhodniini species was required to

test biogeographical patterns, and the areas of endemism

proposed by Amorim (in press) (Fig. 2) were used to produce

a derived-area cladogram to show the historical connections

among the taxa studied and the endemic areas.

In the biogeographical context, the four events used in most

of the models were (1) vicariance, allopatric speciation caused

by the origin of a dispersal barrier affecting many organisms

simultaneously; (2) duplication (speciation within an area),

which is usually allopatric and associated with a local or

temporary dispersal barrier within an area; (3) dispersal,

occurring between isolated areas and associated with speci-

ation; and (4) extinction, which leads to the disappearance of a

lineage from an area where it was predicted to occur

(Sanmartın & Ronquist, 2004).

The reconstruction can best be illustrated by using a

trackogram that displays the organisms’ phylogeny on top of

the area cladogram, with symbols denoting the four kinds of

event. Historical associations can be divided into three basic

categories (Page & Charleston, 1998): genes and organisms;

organisms and organisms; and organisms and areas. Similar-

ities among the event categories for the different kinds of

association need not imply close analogies among the proces-

ses; rather the analogy is among the patterns these processes

produce. Page & Charleston (1998) acknowledged that

equivalent processes among different associations could be

applied to historical biogeography. Following their view, ‘host–

associate’ can be accepted as ‘organism–area’; ‘codivergence’ as

‘vicariance’; ‘duplication’ as ‘sympatry’; ‘host transfer’ as

‘dispersal; and ‘sorting event’ as ‘extinction’.

The reconciled trees used in the previous versions of

TreeMap have some limitations, the most severe being that

they do not accommodate horizontal transfer (dispersal).

Charleston (1998) developed a solution to this problem that

employs a mathematical structure called ‘jungles’, which

contains all possible ways in which an associate tree (¼ taxa)

can be mapped into a host tree (¼ areas), given the four

processes of codivergence, duplication, sorting and horizontal

transfer. This was implemented in TreeMap (Jungle Edition)

ver. 2.02 (Charleston & Page, 2001) and the program was used

to deduce taxon–area associations in our study. The optimal

solutions to explain the biogeographical hypothesis of the

Rhodniini in the Neotropics were those with lowest total cost

(Charleston, 1998).

Information from the studies of van der Hammen (1974),

Clapperton (1993), Hallam (1994), Lundberg et al. (1998),

Aleman & Ramos (2000) and Ramos & Aleman (2000) were

accessed to fit the phylogenetic hypothesis to the geological

events related to the historical distribution of the species

studied here.

RESULTS

Systematics

Parsimony and ML analyses of 16S rDNA sequences included

14 species of Rhodniini and five species of predatory

Reduviidae, representing five of the predatory subfamilies:

Stenopodainae, Ectrichodiinae, Harpactorinae, Reduviinae and

Salyavatinae.

The branch-and-bound search under gap-opening/gap-

extension penalties 15/9, 15/6, 15/3, 9/6, 9/3, 6/3, and using

the outgroup above, resulted in 12 optimal trees (Table 2). The

strict consensus tree for these 12 trees is shown in Fig. 3a. All

the retained trees had the same topology except for the clade

including R. brethesi, R. colombiensis and R. pictipes, which

was unsolved in the strict consensus. Maximum-likelihood

analysis under the same gap penalties resulted in eight trees

(Table 3): the strict consensus of these is shown in Fig. 3b.

Unlike the MP analysis, the strict consensus from the trees

retained in the ML did not show resolution for most of the

Rhodniini species, except for the clade including R. brethesi,

R. stali and R. pictipes. To compare both results of the strict

consensus and combine their resolution, the topology from the

Table 2 Parsimony branch-and-bound search results

GO/GE BP PBP „ TREE L CI RI RC HI

15/9 547 144 3 545 0.607 0.565 0.343 0.393

15/6 550 139 3 524 0.620 0.569 0.353 0.380

15/3 550 136 1 515 0.617 0.563 0.348 0.383

9/6 551 134 1 502 0.620 0.573 0.355 0.380

9/3 554 129 1 491 0.623 0.580 0.362 0.377

6/3 560 129 3 474 0.631 0.593 0.374 0.369

GO/GE, gap-opening/gap-extension penalties; BP, total characters;

PBP, parsimony-informative characters; „ TREE, number of trees

retained; L, length; CI, consistency index; RI, retention index; RC,

rescaled consistency index; HI, homoplasy index.



retained trees was chosen using the alignments 15/3, 9/6 and

9/3 (Fig. 4). Parsimony bootstrap values were obtained for the

alignments 9/6 and 9/3, the consistency indexes of which were

0.620 and 0.623, respectively (Fig. 4). Only Rhodnius domes-

ticus and the clade including Psammolestes species did not

show bootstrap values over 50%. The members of these genera

are morphologically very distinct, and our study suggests that

Psammolestes should be included in the genus Rhodnius.

The outgroup species did not show any sister-group

relationship with the Rhodniini, so that no hypothesis could

be provided to explain the relationship between this tribe and

the subfamilies of Reduviidae. The inclusion of additional

subfamilies of Reduviidae as outgroups in future studies could

resolve this question, although Paula et al. (2005) postulated

an apparent link between Rhodniini, Salyavatinae and Harp-

actorinae.

Biogeography

The distributions of Rhodniini species in the Neotropical

region are shown in Figs 5 and 6, with R. ecuadoriensis,

R. pallescens and R. colombiensis to the west, and R. brethesi,

R. pictipes and R. stali to the east of the Andes (Fig. 5). The

ranges of Rhodnius neivai and R. domesticus are widely

separated, the former occurring in northern South America

and the latter in Atlantic forest in the south-east of the

continent (Fig. 6). Both P. tertius and P. coreodes are found in

south-east South America (Fig. 6), while R. nasutus is restric-

ted to arid regions in the north-east of the continent;

R. prolixus occurs throughout South and Central America;

R. neglectus appears to be restricted to the Serra do Mar and

Serra da Mantiqueira; and R. robustus is widespread in the

Amazon basin (Fig. 6).

An area cladogram for the species of Rhodniini is shown in

Fig. 7, as it is not possible to observe an unambiguous

vicariant pattern for all the species. The first clade, including

R. colombiensis, R. ecuadoriensis and R. pallescens, showed the

latter two species to be sympatric in the Andean/Mesoameri-

can (AnMA) area (Amorim & Pires, 1996). The presence of

R. colombiensis in north-western Amazonia (NWAm) is prob-

ably the result of a vicariance event in the north-west

Neotropical region (Fig. 2), and suggests speciation by vica-

riance following the Andean and Central American uplifts. The

next clade links R. brethesi, R. stali and R. pictipes, three

species with wide geographical ranges overlapping more than

one endemic area, and does not provide a robust explanation

of the biogeographical history of these species in the

Neotropics. Rhodnius neivai occurs in the NWAm area and

R. domesticus in the Atlantic Forest (AtlFor). The species

P. tertius, P. coreodes and R. nasutus are found in AtlFor and

speciated by duplication (paralogy) in this region. Rhodnius

prolixus and R. robustus appear to have dispersed from the

AtlFor, while R. neglectus also appear to have arisen by

duplication in the AtlFor (Fig. 7).

The tanglegram in Fig. 8 shows the relationship between the

areas of endemism proposed by Amorim (in press) and the

phylogeny of the Rhodniini species studied.

Figure 3 (a) Strict consensus tree from

parsimony branch-and-bound searches

resulting in 12 retained trees; (b) strict con-

sensus tree from maximum-likelihood sear-

ches resulting in eight retained trees – in both

cases, total number of trees retained in all

alignments (see Tables 2 & 3).

Table 3 Maximum-likelihood results using the strict consensus

tree retained by parsimony branch-and-bound searches

GO/GE „ TREE )ln L T/T Time

15/9 1 3053.47534 1.60428 06:14.9

15/6 1 2970.87875 1.68883 03:38.5

15/3 1 2936.86807 1.75882 07:06.9

9/6 3 2891.43064 1.86062 10:20.2

9/3 1 2864.50300 1.93612 05:40.6

6/3 1 2811.05100 2.05809 05:50.0

GO/GE, gap opening/gap extension penalties; „ TREE, number of

trees retained; )ln L, likelihood scores; T/T, transition/transversion

ratio; Time, time used (h).



TreeMap 2.02 (Charleston & Page, 2001), with codiver-

gence (vicariance) events weighted as 0 and duplication

(sympatry), lineage losses (extinction) and host switching

(dispersal) all weighted as 1 found 20 scenarios to explain the

biogeographical history of Rhodniini in the Neotropical

region (Table 4). The 12 optimal solutions with the lowest

total cost to explain the biogeographical hypothesis of the

Rhodniini are shown in Fig. 9 (reconstructions 5–16 in

Table 4). These optimal reconstructions require six vicariance

events (black circles), 20 duplications (sympatry; squares), at

least three dispersals (arrows) and at least one extinction

event (grey circles).

TreeMap provided several patterns to explain the species/

area relationships of Rhodniini; thus R. ecuadorensis showed a

vicariance event in the AnMA (Fig. 9a–h) and became extinct

in the NWAm + SWAm (Fig. 9i–l), while R. pallescens

dispersed from NWAm to AnMA (Fig. 9a–d), or speciated

by vicariance when the R. ecuadoriensis lineage disappeared

from those areas (Fig. 9i–l).

This can be explained by the uplift of the Isthmus of

Panama acting as a vicariance event that allowed the

lineage, including R. ecuadoriensis and R. pallescens, to

spread. R. colombiensis dispersed from NWAm (Fig. 9a–d)

and became extinct in the SWAm area (Fig. 9a–l). The

history of the lineage, including R. brethesi, R. pictipes

and R. stali, is puzzling. TreeMap indicated vicariance of

R. brethesi in NWAm and also of R. stali in SWAm, whereas

R. pictipes could have arisen through vicariance in NWAm.

This seems the most robust scenario to explain the present-

day geographical distribution of these species. All the

solutions showed R. neivai in the AnMA endemic area

following dispersal of the lineage R. domesticus–R. neglectus

from AnMA. This clade showed duplication (speciation by

sympatry) in AtlFor, followed by dispersal of R. prolixus and

R. robustus to NWAm, or dispersal of R. neglectus from

NWAm to AtlFor. This last solution deserves more study to

explain the presence of R. prolixus in AtlFor, which has been

interpreted by several epidemiologists as being due to

laboratory escapes. TreeMap could elucidate the biogeo-

graphical history of the Rhodniini more effectively if more

taxa and areas were included to generate the ‘jungles’.

DISCUSSION

Systematics

We refute the idea of an ancestral triatomine similar to extant

Stenopodainae, as well as R. pictipes being the species closest to

the ancestor of Rhodnius, as proposed by Schofield & Dujardin

(1999). Although the sister group of Rhodnius may be the

Salyavatinae or Harpactorinae (Paula et al., 2005), there is still

no conclusive evidence to support this.

According to Schaefer (2005), the main problems to be

resolved in triatomine systematics are whether the subfamily

has a truly independent origin and how it is related to the

other subfamilies of the Reduviidae. We currently have no

idea which of these subfamilies is most closely related to the

Triatominae. The surprisingly few studies of reduviid

subfamilies have allied the Triatominae with the Harpactor-

inae, Peiratinae, Physoderinae, Reduviinae and Stenopodai-

nae.

Ambrose (1999) suggested that the reduviids could be

broadly divided into two groups based on whether or not

they possessed tibial pads (fossulae espongiosae, or tibiarola).

Reduviids with tibial pads may have evolved in the following

sequence: Holoptilinae, Emesinae, Tribelocephalinae, Saici-

nae, Stenopodainae, Harpactorinae. Those without tibial pads

live in tropical forest ecosystems and are known as timid

predators that do not use their forelegs to capture prey,

instead impaling prey items with their long rostra (Ambrose,

1999). Rain forest reduviids may have developed tibial pads

and other features that made them more efficient predators

when they migrated to deciduous scrub forest and other

semi-arid habitats. The most advanced, aggressive predators,

such as members of the Peiratinae and Reduviinae, live in

Figure 4 Selected topology from parsimony branch-and-bound

search to show the phylogenetic hypothesis for the relationship

among Rhodniini species. Numbers above and below branches are

bootstrap support; frequencies ‡ 50%. Gap-opening/gap-exten-

sion penalties were 9/6 and 9/3, respectively, and are shown above

and below the branches.



semi-arid, prey-scarce situations where such features would

be most needed.

The Salyavatinae possess the least developed tibial pads,

which may be rudimentary, consist of mere apical projections

or be distinctly formed. Ambrose (1999) considered the

members of this subfamily to be the most primitive of the

predatory reduviids, ancestral to the subfamilies Triatominae

and Ectrichodiinae (see his Figure 54). Although the Rhodniini

and Salyavatinae could have shared the same Neotropical

ancestor, the results of our study do not provide sufficient

evidence to corroborate this. An alternative, and possibly more

robust hypothesis, is that the Rhodniini and Harpactorinae are

closely related.

Biogeography

Vicariance and dispersalist schools of biogeographical analysis

are both compatible with the dominance of allopatric speci-

ation, but differ in how they construe the interaction between

dispersal and allopatry. In the vicariance paradigm, rare but

extensive dispersal (range expansion) is followed by a series of

allopatric isolation events, interrupted by occasional random

Figure 5 Known distribution of Rhodniini species in South and Central America. See text for data sources.



dispersals (Zink et al., 2000). If the isolation events affect many

organisms simultaneously, this process will generate congruent

tree topologies. Dispersalists consider range expansion to be a

more common and regularly occurring phenomenon. Both

dispersal and vicariance processes are viewed as possibly

resulting in predictable as well as unpredictable (random)

events. Conflicting or incongruent trees can be explained by

differential dispersal across pre-existing barriers. Trees may

also appear to conflict if they have unequal numbers of

terminal taxa, which can result from failure of differentiation

in response to a barrier (widespread species), or because some

lineages have experienced extinctions. However, such trees can

be compatible with vicariance. The strongest statements about

dispersal events can be made when they are rare and mixed

with vicariance between areas of endemism. Under such

conditions, there will be strong phylogenetic constraints on

distributional patterns.

Humphries & Ebach (2004) discussed the current state of

cladistic biogeography and highlighted two critical points that

require investigation: the definition of endemic areas and

geographical congruence. Many other authors have discussed

the concepts of endemic areas (Nelson & Platnick, 1981;

Platnick, 1991; Harold & Mooi, 1994; Morrone, 1994;

Humphries & Parenti, 1999; Hausdorf, 2002) without reaching

Figure 6 Known distribution of Rhodniini species in South and Central America. See text for data sources.



a consensus. Cox & Moore (2005) pointed out that some

plants and animals are confined to the areas in which they

evolved and are said to be endemic to that region. Their

confinement may be due to physical barriers to dispersal, as in

the case of many island faunas and floras (palaeoendemics), or

to the fact that they have evolved only recently and have not

yet had time to spread (neoendemics). The concept of endemic

areas requires more investigation and discussion, although

Amorim & Pires (1996) and Amorim (2001, in press) have

published interesting papers on the delimitation of endemic

areas in the Neotropics. Similar vicariance patterns have been

postulated for Coleoptera (Morrone, 2002) and Diptera (Nihei

& Carvalho, 2004).

Vicariance-induced and dispersion-induced elements

explain the present diversity of the Neotropical region

(Amorim, in press). Congruence of the distributions of

different groups of organisms and the Cretaceous–Tertiary

Figure 8 Tanglegram showing relationship between areas of

endemism and phylogeny of Rhodniini species. Areas of ende-

mism as proposed by Amorim (in press).

Table 4 Twenty optimal reconstructions satisfying the following

event costs constraints: codivergences, 0; host switches, 1; dupli-

cations, 1; losses, 1

No. C D L S E z

1 4 22 0 6 28 28

2 4 22 0 6 28 28

3 4 22 0 6 28 28

4 4 22 0 6 28 28

5 6 20 1 5 26 26

6 6 20 1 5 26 26

7 6 20 2 4 26 26

8 6 20 2 4 26 26

9 6 20 1 5 26 26

10 6 20 1 5 26 26

11 6 20 2 4 26 26

12 6 20 2 4 26 26

13 6 20 2 4 26 26

14 6 20 2 4 26 26

15 6 20 3 3 26 26

16 6 20 3 3 26 26

17 6 20 8 2 30 30

18 6 20 8 2 30 30

19 6 20 15 1 36 36

20 6 20 20 0 40 40

No., reconstruction number; C, number of codivergence events

(vicariance); D, number of duplication events (sympatry); L, number

of losses (extinction); S, number of host switch events (dispersal); E,

total number of non-codivergence events; z, total cost.

a b

Figure 7 Area cladogram of Rhodniini species using areas of endemism proposed by Amorim (in press) for the Neotropical region.



a b c

d e f

g h i

j k l

Figure 9 Twelve optimal reconstructions with the lowest cost for the tanglegram shown in Fig. 8. Vicariance events (d); duplications

(sympatry) (j); dispersals (arrows); extinction events (d).



geological history of the Neotropical region point to a number

of vicariance events having caused the disjunction patterns

observed today (Fig. 2). Most events were associated with

tectonic movements and inundations, with long-term and

local dispersions also having some impact.

A general pattern shows a separation between Caribbean–

Antillean elements from a continental Neotropical component,

followed by a division between the south-east Amazonia–

Atlantic Forest and north-west South America–Central Amer-

ica components (Fig. 2). Other, more regional events follow.

There is evidence of repeated inundation of the Neotropical

region that may have resulted in vicariance events in the

Cretaceous as well as the Eocene, Miocene and Pleistocene

epochs of the Quaternary period (Amorim, in press).

Amorim & Pires (1996) and Amorim (2001, in press)

showed many more endemic areas in the Neotropical region,

but lacked information to reconstruct their histories. Accord-

ing to these authors, additional studies are needed to add new

areas of endemism; subdivide some existing areas into smaller

units (e.g. AnMA, SWAm); and establish a sequence for area

components that can be subdivided into polytomies (as for

SWAm).

Although the Neotropical region may conveniently be

considered as a single biogeographical unit, it is geologically

complex. The Neotropics include not only the South American

continental plate, but also the southern portion of the North

American and Caribbean plates (Clapperton, 1993). The

complicated geological history of the region, in which these

plates intermittently separated and collided throughout the

Cretaceous and the Tertiary, provides the milieu within which

interactions between organisms have occurred. South America

has been an island continent for most of the evolutionary

history of some organisms (e.g. angiosperms), whereas Central

America constitutes one of the two tropical parts of the

Laurasian ‘supercontinent’. The outstanding geological feature

of South America is the Andes, the longest mountain range in

the world. Andean tectonic history is extremely important in

understanding biogeographical process and pattern. It is now

known that the Andes were built by compressional tectonics

during the last 90 Myr or even longer. It is, therefore, overly

simplistic to view Andean vicariance as a singular event

occurring with the Miocene uplift (Lundberg et al., 1998).

The Andes essentially represent a classical tectonic upthrust

of continental rock, the result of a collision between the

leading edge of the westward-moving South American and

oceanic Pacific Plates (Lundberg et al., 1998). The southern

Andes are the oldest, with significant uplift already present in

the early Cenozoic, prior to the Oligocene. Most of the uplift of

the Central Andes was in the Miocene or later, whereas that

of the northern portion of the range was mostly Plio-

Pleistocene (van der Hammen, 1974). Rhodnius ecuadoriensis

could have speciated following the Central Andean uplift.

As they extend northwards the Andes become more

geologically complex, breaking into three separate cordilleras

(Aleman & Ramos, 2000). The Western and Central Cordil-

leras of the Andes are typical subduction-related mountain

chains developed along the continental margin. However, the

Eastern Cordillera was formed as a result of the interaction

between the Paleogene Caribbean thrusting and Neogene

tectonic inversion during Andean compression. These struc-

tures were greatly affected by a complex system of strike–slip

faults and folds. We think that the break-up of the Andes into

three separate cordilleras was a geological event leading to the

evolution of R. colombiensis, R. brethesi and R. neivai within

their respective geographical ranges.

The major geological events believed to have occurred at the

intersection of South, Central and North America are

described by Hallam (1994). In the Jurassic, North and South

America were joined and Central America as we know it today

did not exist. In the early Cretaceous, North and South

America separated just to the south of the Yucatan peninsula.

Volcanic islands subsequently appeared in the gap between

southern Mexico and Colombia. These were pushed north-

eastwards by the Farallon Plate, which in the mid-Cretaceous

began to form Cuba, the Greater Antilles and the islands off the

Venezuelan coast. By the early Oligocene, another archipelago

had been created between South and North America, the

widest gap between islands being in the Panama region. The

land corridor between South and North America was com-

pleted in the Pliocene with the emergence of the Isthmus of

Panama and north-west Colombia. Rhodnius pallescens occurs

only in Central America and could only have speciated after

the isthmus was formed.

The Serra do Mar and Serra da Mantiqueira mountain

systems are younger than the Andes, having formed between

the Oligocene and Pleistocene (Amorim & Pires, 1996). The

results of our study indicate that many duplication events

(speciations within an area) occurred in AtlFor. As these events

are usually allopatric and associated with a local or temporary

dispersal barrier within an area, the uplift of the Serra do Mar

and Serra da Mantiqueira could have resulted in the speciation

of R. domesticus, P. tertius, P. coreodes and R. nasutus. Uplift

of these mountains may also explain the origin and dispersal of

R. prolixus and R. robustus from AtlFor.

Pinho et al. (1998) collected R. prolixus in Atlantic rain

forest near Teresopolis, in the Serra do Mar. The specimens

(adults, nymphs and eggs) were found in the axils of

Pteridophyta leaves, in foliage and on the trunks of palm

trees. This was the first report of Rhodnius colonizing

Pteridophyta, and some researchers have suggested that these

insects were descended from escaped laboratory-bred speci-

mens. Based on previous studies and our own findings (Fig. 9),

R. prolixus could have speciated in the Atlantic Forest of the

Serra do Mar, following dispersal to north-west South America

and Central America. The distribution of this species in the

Serra do Mar should be studied further as it is the main target

of Chagas’ disease vector control initiatives.

CONCLUSIONS

The Rhodniini have a complex biogeographical history that

has involved vicariance, duplications (sympatry), dispersal and



extinction events. The main geological events affecting the

origin and diversification of the Rhodniini in the Neotropics

were: (1) uplift of the Central Andes in the Miocene or later,

(2) break-up of the Andes into three separate cordilleras

(Eastern, Central and Western) in the Plio-Pleistocene, (3)

formation of a land corridor connecting South and North

America in the Pliocene, and (4) uplift of the Serra do Mar and

Serra da Mantiqueira mountain systems between the Oligocene

and Pleistocene. The relationships and biogeographical history

of the species of Rhodniini to the Neotropical region probably

arose from the areas of endemism proposed by Amorim (2001,

in press).

ACKNOWLEDGEMENTS

We thank Dr Carl Schaefer (University of Connecticut) and

Dr Thomas Henry (Smithsonian Institution) for comments

on an early version of the manuscript. Dr Dalton de Souza

Amorim (Faculdade de Filosofia, Ciencias e Letras de Ribeirao

Preto/USP) provided us with figures from his studies (Figs 1

& 2). Dr Gustavo Graciolli (Universidade Federal de Mato

Grosso do Sul) commented on the TreeMap results. Dr Malte

C. Ebach, Dr Juan J. Morrone and Dr John Grehan made

constructive criticisms in reviewing our manuscript. Dr Bruce

Alexander (Liverpool School of Tropical Medicine) made the

English revision and provided comments that improved our

manuscript. The study was supported by grants from the

Centro de Pesquisas Rene Rachou/FIOCRUZ, Fundacao de

Amparo a Pesquisa de Minas Gerais (FAPEMIG), and

Conselho Nacional de Desenvolvimento Cientıfico e Tec-

nologico (CNPq).

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BIOSKETCHES

Alexandre Silva de Paula has a DS in Entomology from

Universidade Federal de Vicosa, Brazil. His research focuses on

the systematics and biogeography of Triatominae. He teaches

Systematics at Centro de Pesquisas Rene Rachou/FIOCRUZ.

Lileia Diotaiuti has a DS in Parasitology from Universidade

Federal de Minas Gerais, Brazil. Her research focuses on

Chagas disease vectors control in Latin America. She teaches

Biology and Control of Triatominae, and Scientific Methodo-

logy at Centro de Pesquisas Rene Rachou/FIOCRUZ.

Cleber Galvao has a DS in Veterinary Science from

Universidade Federal Rural do Rio de Janeiro, Brazil. His

research focuses on biology, systematics and comparative

morphology of Triatominae. He teaches Medical Entomology

and Protozoology at Instituto Oswaldo Cruz/FIOCRUZ.

Editor: Malte C. Ebach



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