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

ORIGINAL Systematics and biogeography of ARTICLE Rhodniini (: : Triatominae) based on 16S mitochondrial rDNA sequences Alexandre Silva de Paula1*, Lile´ia Diotaiuti1 and Cleber Galva˜o2

1Laborato´rio de Triatomı´neos e Epidemiologia ABSTRACT da Doenc¸a de Chagas, Centro de Pesquisas Aim The tribe Rhodniini is one of six comprising the subfamily Triatominae Rene´ Rachou/FIOCRUZ, Av. Augusto de Lima 1715, 30190-002 Belo Horizonte, MG and (Heteroptera: Reduviidae), notorious as blood-sucking household pests and 2Laborato´rio Nacional e Internacional de vectors of Trypanosoma cruzi throughout Latin America. The human and Refereˆncia em Taxonomia de Triatomı´neos, economic cost of this disease in the American tropics is considerable, and these Departamento de Protozoologia, Instituto bugs are unquestionably of great importance to man. Studies of the evolution, Oswaldo Cruz/FIOCRUZ, Av. Brasil 4365, phylogeny, biogeography, ecology, physiology and behaviour of the Rhodniini are 21040-900 Rio de Janeiro, RJ, Brazil 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. *Correspondence: Alexandre Silva de Paula, Laborato´rio de Triatomı´neos e Epidemiologia Main conclusions The Rhodniini have a complex biogeographical history that ´ da Doenc¸a de Chagas, Centro de Pesquisas Rene has involved vicariance, duplications (sympatry), dispersal and extinction events. Rachou/FIOCRUZ, Av. Augusto de Lima 1715, 30190-002 Belo Horizonte, MG, Brazil. The main geological events affecting the origin and diversification of the E-mail: alex@cpqrr.fiocruz.br Rhodniini in the Neotropics were (1) uplift of the Central Andes in the Miocene

ª 2006 The Authors www.blackwellpublishing.com/jbi 699 Journal compilation ª 2006 Blackwell Publishing Ltd doi:10.1111/j.1365-2699.2006.01628.x A. S. Paula, L. Diotaiuti and C. Galva˜ o

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, , historical biogeography, Neotropical, Psammolestes, rDNA mitochondrial gene, , Triatominae.

with other mammals; as such they are not important in INTRODUCTION T. cruzi transmission (Lent & Wygodzinsky, 1979). The tribe Rhodniini Pinto, 1926 is one of six comprising the The importance of the Rhodniini lies in the fact that some of subfamily Triatominae (Heteroptera: Reduviidae), notorious its members feed on humans and many of these transmit as blood-sucking household pests and vectors of Trypanosoma T. cruzi, the protozoan that causes Chagas’ disease. The human cruzi Chagas, 1909 throughout the Neotropics (Galva˜o et al., and economic costs of this disease in the American tropics are 2003). Their genera belong to a well defined monophyletic considerable (Schaefer, 2005). group (Lent & Wygodzinsky, 1979). Morphological characters A wide variety of reasons have been proposed for the high can be used to distinguish Rhodnius Sta˚l, 1859 and Psammo- biological diversity seen in the Neotropics (Amorim, in press). lestes Bergroth, 1911, the two genera of Rhodniini, particularly Accepted causes of disjunction include: (1) tectonic displace- the apically inserted antennae and the presence of distinct ment, (2) sea-level fluctuations, (3) interspecific competition callosities behind the eyes (Lent & Wygodzinsky, 1979). together with climate change, (4) parapatric speciation along Species of Rhodnius are primarily arboreal, often occupying environmental gradients, (5) pest pressure, and (6) fine-scale ecotopes in palm tree crowns or epiphytic bromeliads. The habitat heterogeneity (for details see Amorim, 2006). genus is widely distributed in South and Central America. In The first two of these causes are classed as palaeogeograph- Central America and the northern Andean countries (Peru, ical, being Mesozoic–Lower Tertiary events, while the latter Ecuador, Colombia and Venezuela), Rhodnius species are four occurred mainly in the Quaternary. Some of them primary targets of Chagas’ disease vector control initiatives. represent competing explanations for the same biological This is particularly true for Rhodnius prolixus Sta˚l, 1872, as well events. Most of the causes proposed for species diversification as Rhodnius ecuadoriensis Lent & Leo´n, 1958 in parts of in these models were not inferred based on a given method of Ecuador and northern Peru and Rhodnius pallescens Barber, biogeographical reconstruction, but rather were chosen a pri- 1932 in Panama and parts of Colombia. Other Rhodnius ori based on other sources of evidence (Amorim, in press). species have local epidemiological importance, including Several Neotropical groups of organisms have species that Rhodnius neglectus Lent, 1954 and Rhodnius nasutus Sta˚l, are widely distributed throughout South and Central America 1859 in central and northeastern Brazil; Rhodnius stali Lent (Amorim, in press). However, groups as divergent as mammals et al., 1993 in Bolivia; and Rhodnius brethesi Matta, 1919 in the and also contain species with restricted and overlapping Brazilian Amazon (Schofield & Dujardin, 1999). The genus geographical distributions. The areas of endemism proposed Rhodnius was reviewed by Lent (1948), Lent & Jurberg (1969), by dispersionists, refuge theory biogeographers and vicariance Lent & Wygodzinsky (1979). Three additional species have biogeographers, based on studies of different groups such as since been described: R. stali (Lent et al., 1993), Rhodnius insects, arachnids, mammals and plants, are largely congruent. colombiensis (Moreno et al., 1999) and Rhodnius milesi Thus, despite disagreements about the causes of cladogeneses, (Valente et al., 2001). The genus Rhodnius currently has 16 different biogeographical schools largely concur regarding the recognized species, including Rhodnius dalessandroi Carcavallo boundaries of the main areas of endemism in the Neotropics & Barreto, 1976 and Rhodnius paraensis Sherlock et al., 1977, (Fig. 1). This strongly suggests common causes for the origin neither of which has been collected since its original descrip- of these patterns. tion. Methods that allow for both dispersal and vicariance have The genus Psammolestes includes Psammolestes arturi been proposed to reconstruct biogeographical history (Pinto), 1926, Psammolestes coreodes Bergroth, 1911 and (Ronquist, 1997). Hence there is a growing plurality in the Psammolestes tertius Lent & Jurberg, 1965 (Galva˜o et al., theoretical and methodological tools of biogeography. Never- 2003). The genus was reviewed by Lent & Jurberg (1965) and theless, few empirical studies have documented the relative Lent & Wygodzinsky (1979). Species of Psammolestes live in roles of vicariance and dispersal (Zink et al., 2000). The aim of birds’ nests. They do not associate with man, and only rarely the study reported here was to formulate biogeographical

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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, Cieˆncias e Letras de Ribeira˜o Preto/ USP; see Amorim & Pires, 1996). hypotheses to explain the modern geographical distribution of represented by unequal taxon sets in the construction of the Rhodniini species. Both systematic and biogeographical outgroup. Initial analyses were made by aligning groups of approaches were used to construct testable hypotheses, using sequences using ClustalX 1.83 (Thompson et al., 1997) under area cladograms (Cracraft, 1994) and the program TreeMap gap-opening/gap-extension penalties 15/9, 15/6, 15/3, 9/6, 9/3, 2.02 (Charleston & Page, 2001). The biogeographical hypoth- 6/3, and by treating the gaps as missing (?). The analyses esis was formulated using Amorim’s (in press) historical included the available 16S sequences from predatory reduviid reconstruction of the Neotropical region (Fig. 2). subfamilies present in GenBank as an outgroup: Stenopoda spinulosa Giacchi, 1969 (Stenopodainae); Ectrychotes andreae (Thunberg), 1784 (Ectrichodiinae); Sycanus croceus Hsiao, METHODS 1979 (Harpactorinae); Tiarodes venenatus Matsumura, 1913 (Reduviinae); Lisarda rhypara Sta˚l, 1858 (Salyavatinae) Systematics (Table 1). The outgroup was chosen based on the findings of In the present study we used mitochondrial rDNA sequences Paula et al. (2005) and the fact that the ancestral form of (16S) currently available in the NCBI genetic database. Other Rhodnius was placed in the Stenopodainae by Schofield & genes currently available in the NCBI database (e.g. 12S, Dujardin (1999). cytochrome oxidase 1, cytochrome b, and nuclear rDNA The species R. dalessandroi, R. paraensis, Rhodnius amazo- sequences 18S and ITS2) were not considered because of the nicus, R. milesi and P. arturi were not included in this analysis methodological difficulties of combining sequence information because there were no gene sequences for them in GenBank. from different genes (Kitching et al., 1998; Sanderson & Cladistic analysis used the program PAUP 4.0b10 (Swofford, Shaffer, 2002), and the fact that different genes were 2002) to derive trees based on maximum parsimony (MP) and

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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, Cieˆncias e Letras de Ribeira˜o Preto/USP; Amorim, in press).

Table 1 Species and 16S ribosomal DNA Taxa Accession no. Length %GC gene (mitochondrial gene) sequences used in maximum parsimony and maximum likeli- Outgroup hood analyses 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 Sta˚l, 1858 AY127039 508 29.0 Ingroup Rhodnius pallescens Barber, 1932 AF045706 374 24.0 Rhodnius ecuadoriensis Lent & Leo´n, 1958 AF028746 285 23.0 Rhodnius colombiensis Mejia, Galva˜o & Jurberg, 1999 AY035438 510 28.0 Rhodnius pictipes Sta˚l, 1872 AF045709 373 26.0 Rhodnius stali Lent, Jurberg & Galva˜o, 1993 AY035437 508 29.0 Rhodnius prolixus Sta˚l, 1859 AF045707 373 27.0 Rhodnius nasutus Sta˚l, 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. maximum likelihood (ML). Parsimony branch-and-bound branch-and-bound search. Parsimony bootstrap analyses were searches were performed on the alignments using the chosen conducted employing a heuristic search with 100 bootstrap outgroup. Characters were treated as unordered and of equal replicates using 10 random stepwise addition (tree-bisection- weight, and the trees were rooted at an internal node with basal reconnection, TBR). Strict consensus trees were obtained from polytomy. Strict consensus trees were then obtained for each all the retained trees in the branch-and-bound searches, and

702 Journal of Biogeography 34, 699–712 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd Systematics and biogeography of Rhodniini the topology of each tree under individual gap-opening/gap- Charleston (1998) developed a solution to this problem that extension penalties was tested with ML, using a model of employs a mathematical structure called ‘jungles’, which estimated gamma distribution (discrete approximation), contains all possible ways in which an associate tree (¼ taxa) HKY85 variant to allow for transition/transversion bias, can be mapped into a host tree (¼ areas), given the four unequal base frequencies and different substitution rates (Page processes of codivergence, duplication, sorting and horizontal & Homes, 1998), empirical base frequencies and an estimated transfer. This was implemented in TreeMap (Jungle Edition) substitution model following heuristic stepwise addition using ver. 2.02 (Charleston & Page, 2001) and the program was used TBR branch-swapping. 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 Biogeography (Charleston, 1998). Distributional data for Rhodnius species were obtained from Information from the studies of van der Hammen (1974), reviews by Lent (1948), Lent & Jurberg (1969), Lent Clapperton (1993), Hallam (1994), Lundberg et al. (1998), & Wygodzinsky (1979). Additional localities for R. stali, Aleman & Ramos (2000) and Ramos & Aleman (2000) were R. colombiensis, R. milesi and R. amazonicus were obtained accessed to fit the phylogenetic hypothesis to the geological from Lent et al. (1993), Moreno et al. (1999), Valente et al. events related to the historical distribution of the species (2001) and Be´renger & Pluot-Sigwalt (2002), respectively. studied here. Distributional data for Psammolestes species were obtained from Lent & Jurberg (1965) and Lent & Wygodzinsky (1979). RESULTS Coordinates of the localities were obtained from Vanzolini & Papavero (1969) and Brown (1979). Species distributions were Systematics plotted on maps of South and Central America using the program iMap 3.1 for Apple Macintosh. Parsimony and ML analyses of 16S rDNA sequences included Phylogenetic analysis of Rhodniini species was required to 14 species of Rhodniini and five species of predatory test biogeographical patterns, and the areas of endemism Reduviidae, representing five of the predatory subfamilies: proposed by Amorim (in press) (Fig. 2) were used to produce Stenopodainae, Ectrichodiinae, Harpactorinae, Reduviinae and a derived-area cladogram to show the historical connections Salyavatinae. among the taxa studied and the endemic areas. The branch-and-bound search under gap-opening/gap- In the biogeographical context, the four events used in most extension penalties 15/9, 15/6, 15/3, 9/6, 9/3, 6/3, and using of the models were (1) vicariance, allopatric speciation caused the outgroup above, resulted in 12 optimal trees (Table 2). The by the origin of a dispersal barrier affecting many organisms strict consensus tree for these 12 trees is shown in Fig. 3a. All simultaneously; (2) duplication (speciation within an area), the retained trees had the same topology except for the clade which is usually allopatric and associated with a local or including R. brethesi, R. colombiensis and R. pictipes, which temporary dispersal barrier within an area; (3) dispersal, was unsolved in the strict consensus. Maximum-likelihood occurring between isolated areas and associated with speci- analysis under the same gap penalties resulted in eight trees ation; and (4) extinction, which leads to the disappearance of a (Table 3): the strict consensus of these is shown in Fig. 3b. lineage from an area where it was predicted to occur Unlike the MP analysis, the strict consensus from the trees (Sanmartı´n & Ronquist, 2004). retained in the ML did not show resolution for most of the The reconstruction can best be illustrated by using a Rhodniini species, except for the clade including R. brethesi, trackogram that displays the organisms’ phylogeny on top of R. stali and R. pictipes. To compare both results of the strict the area cladogram, with symbols denoting the four kinds of consensus and combine their resolution, the topology from the event. Historical associations can be divided into three basic categories (Page & Charleston, 1998): genes and organisms; organisms and organisms; and organisms and areas. Similar- Table 2 Parsimony branch-and-bound search results ities among the event categories for the different kinds of GO/GE BP PBP „ TREE L CI RI RC HI association need not imply close analogies among the proces- ses; rather the analogy is among the patterns these processes 15/9 547 144 3 545 0.607 0.565 0.343 0.393 produce. Page & Charleston (1998) acknowledged that 15/6 550 139 3 524 0.620 0.569 0.353 0.380 equivalent processes among different associations could be 15/3 550 136 1 515 0.617 0.563 0.348 0.383 applied to historical biogeography. Following their view, ‘host– 9/6 551 134 1 502 0.620 0.573 0.355 0.380 associate’ can be accepted as ‘organism–area’; ‘codivergence’ as 9/3 554 129 1 491 0.623 0.580 0.362 0.377 ‘vicariance’; ‘duplication’ as ‘sympatry’; ‘host transfer’ as 6/3 560 129 3 474 0.631 0.593 0.374 0.369 ‘dispersal; and ‘sorting event’ as ‘extinction’. GO/GE, gap-opening/gap-extension penalties; BP, total characters; The reconciled trees used in the previous versions of PBP, parsimony-informative characters; „ TREE, number of trees TreeMap have some limitations, the most severe being that retained; L, length; CI, consistency index; RI, retention index; RC, they do not accommodate horizontal transfer (dispersal). rescaled consistency index; HI, homoplasy index.

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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 R. pallescens and R. colombiensis to the west, and R. brethesi, tree retained by parsimony branch-and-bound searches R. pictipes and R. stali to the east of the Andes (Fig. 5). The ranges of Rhodnius neivai and R. domesticus are widely GO/GE „ TREE )ln LT/T Time separated, the former occurring in northern South America 15/9 1 3053.47534 1.60428 06:14.9 and the latter in Atlantic forest in the south-east of the 15/6 1 2970.87875 1.68883 03:38.5 continent (Fig. 6). Both P. tertius and P. coreodes are found in 15/3 1 2936.86807 1.75882 07:06.9 south-east South America (Fig. 6), while R. nasutus is restric- 9/6 3 2891.43064 1.86062 10:20.2 ted to arid regions in the north-east of the continent; 9/3 1 2864.50300 1.93612 05:40.6 R. prolixus occurs throughout South and Central America; 6/3 1 2811.05100 2.05809 05:50.0 R. neglectus appears to be restricted to the Serra do Mar and GO/GE, gap opening/gap extension penalties; „ TREE, number of Serra da Mantiqueira; and R. robustus is widespread in the trees retained; )ln L, likelihood scores; T/T, transition/transversion Amazon basin (Fig. 6). ratio; Time, time used (h). 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 retained trees was chosen using the alignments 15/3, 9/6 and R. colombiensis, R. ecuadoriensis and R. pallescens, showed the 9/3 (Fig. 4). Parsimony bootstrap values were obtained for the latter two species to be sympatric in the Andean/Mesoameri- alignments 9/6 and 9/3, the consistency indexes of which were can (AnMA) area (Amorim & Pires, 1996). The presence of 0.620 and 0.623, respectively (Fig. 4). Only Rhodnius domes- R. colombiensis in north-western Amazonia (NWAm) is prob- ticus and the clade including Psammolestes species did not ably the result of a vicariance event in the north-west show bootstrap values over 50%. The members of these genera Neotropical region (Fig. 2), and suggests speciation by vica- are morphologically very distinct, and our study suggests that riance following the Andean and Central American uplifts. The Psammolestes should be included in the genus Rhodnius. next clade links R. brethesi, R. stali and R. pictipes, three The outgroup species did not show any sister-group species with wide geographical ranges overlapping more than relationship with the Rhodniini, so that no hypothesis could one endemic area, and does not provide a robust explanation be provided to explain the relationship between this tribe and of the biogeographical history of these species in the the subfamilies of Reduviidae. The inclusion of additional Neotropics. Rhodnius neivai occurs in the NWAm area and subfamilies of Reduviidae as outgroups in future studies could R. domesticus in the Atlantic Forest (AtlFor). The species resolve this question, although Paula et al. (2005) postulated P. tertius, P. coreodes and R. nasutus are found in AtlFor and an apparent link between Rhodniini, Salyavatinae and Harp- speciated by duplication (paralogy) in this region. Rhodnius actorinae. 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). Biogeography The tanglegram in Fig. 8 shows the relationship between the The distributions of Rhodniini species in the Neotropical areas of endemism proposed by Amorim (in press) and the region are shown in Figs 5 and 6, with R. ecuadoriensis, phylogeny of the Rhodniini species studied.

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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 Figure 4 Selected topology from parsimony branch-and-bound the ancestor of Rhodnius, as proposed by Schofield & Dujardin search to show the phylogenetic hypothesis for the relationship (1999). Although the sister group of Rhodnius may be the among Rhodniini species. Numbers above and below branches are Salyavatinae or Harpactorinae (Paula et al., 2005), there is still bootstrap support; frequencies ‡ 50%. Gap-opening/gap-exten- no conclusive evidence to support this. sion penalties were 9/6 and 9/3, respectively, and are shown above and below the branches. 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 TreeMap 2.02 (Charleston & Page, 2001), with codiver- idea which of these subfamilies is most closely related to the gence (vicariance) events weighted as 0 and duplication Triatominae. The surprisingly few studies of reduviid (sympatry), lineage losses (extinction) and host switching subfamilies have allied the Triatominae with the Harpactor- (dispersal) all weighted as 1 found 20 scenarios to explain the inae, Peiratinae, Physoderinae, Reduviinae and Stenopodai- biogeographical history of Rhodniini in the Neotropical nae. region (Table 4). The 12 optimal solutions with the lowest Ambrose (1999) suggested that the reduviids could be total cost to explain the biogeographical hypothesis of the broadly divided into two groups based on whether or not Rhodniini are shown in Fig. 9 (reconstructions 5–16 in they possessed tibial pads (fossulae espongiosae, or tibiarola). Table 4). These optimal reconstructions require six vicariance Reduviids with tibial pads may have evolved in the following events (black circles), 20 duplications (sympatry; squares), at sequence: Holoptilinae, Emesinae, Tribelocephalinae, Saici- least three dispersals (arrows) and at least one extinction nae, Stenopodainae, Harpactorinae. Those without tibial pads event (grey circles). live in tropical forest ecosystems and are known as timid TreeMap provided several patterns to explain the species/ predators that do not use their forelegs to capture prey, area relationships of Rhodniini; thus R. ecuadorensis showed a instead impaling prey items with their long rostra (Ambrose, vicariance event in the AnMA (Fig. 9a–h) and became extinct 1999). Rain forest reduviids may have developed tibial pads in the NWAm + SWAm (Fig. 9i–l), while R. pallescens and other features that made them more efficient predators dispersed from NWAm to AnMA (Fig. 9a–d), or speciated when they migrated to deciduous scrub forest and other by vicariance when the R. ecuadoriensis lineage disappeared semi-arid habitats. The most advanced, aggressive predators, from those areas (Fig. 9i–l). such as members of the Peiratinae and Reduviinae, live in

Journal of Biogeography 34, 699–712 705 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd A. S. Paula, L. Diotaiuti and C. Galva˜ o

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

semi-arid, prey-scarce situations where such features would robust hypothesis, is that the Rhodniini and Harpactorinae are be most needed. closely related. The Salyavatinae possess the least developed tibial pads, which may be rudimentary, consist of mere apical projections Biogeography or be distinctly formed. Ambrose (1999) considered the members of this subfamily to be the most primitive of the Vicariance and dispersalist schools of biogeographical analysis predatory reduviids, ancestral to the subfamilies Triatominae are both compatible with the dominance of allopatric speci- and Ectrichodiinae (see his Figure 54). Although the Rhodniini ation, but differ in how they construe the interaction between and Salyavatinae could have shared the same Neotropical dispersal and allopatry. In the vicariance paradigm, rare but ancestor, the results of our study do not provide sufficient extensive dispersal (range expansion) is followed by a series of evidence to corroborate this. An alternative, and possibly more allopatric isolation events, interrupted by occasional random

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Figure 6 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 be compatible with vicariance. The strongest statements about organisms simultaneously, this process will generate congruent dispersal events can be made when they are rare and mixed tree topologies. Dispersalists consider range expansion to be a with vicariance between areas of endemism. Under such more common and regularly occurring phenomenon. Both conditions, there will be strong phylogenetic constraints on dispersal and vicariance processes are viewed as possibly distributional patterns. resulting in predictable as well as unpredictable (random) Humphries & Ebach (2004) discussed the current state of events. Conflicting or incongruent trees can be explained by cladistic biogeography and highlighted two critical points that differential dispersal across pre-existing barriers. Trees may require investigation: the definition of endemic areas and also appear to conflict if they have unequal numbers of geographical congruence. Many other authors have discussed terminal taxa, which can result from failure of differentiation the concepts of endemic areas (Nelson & Platnick, 1981; in response to a barrier (widespread species), or because some Platnick, 1991; Harold & Mooi, 1994; Morrone, 1994; lineages have experienced extinctions. However, such trees can Humphries & Parenti, 1999; Hausdorf, 2002) without reaching

Journal of Biogeography 34, 699–712 707 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd A. S. Paula, L. Diotaiuti and C. Galva˜ o

ab

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

Table 4 Twenty optimal reconstructions satisfying the following event costs constraints: codivergences, 0; host switches, 1; dupli- cations, 1; losses, 1

No. CD L SE 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.

yet had time to spread (neoendemics). The concept of endemic Figure 8 Tanglegram showing relationship between areas of areas requires more investigation and discussion, although endemism and phylogeny of Rhodniini species. Areas of ende- Amorim & Pires (1996) and Amorim (2001, in press) have mism as proposed by Amorim (in press). published interesting papers on the delimitation of endemic areas in the Neotropics. Similar vicariance patterns have been a consensus. Cox & Moore (2005) pointed out that some postulated for Coleoptera (Morrone, 2002) and Diptera (Nihei plants and are confined to the areas in which they & Carvalho, 2004). evolved and are said to be endemic to that region. Their Vicariance-induced and dispersion-induced elements confinement may be due to physical barriers to dispersal, as in explain the present diversity of the Neotropical region the case of many island faunas and floras (palaeoendemics), or (Amorim, in press). Congruence of the distributions of to the fact that they have evolved only recently and have not different groups of organisms and the Cretaceous–Tertiary

708 Journal of Biogeography 34, 699–712 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd Systematics and biogeography of Rhodniini

abc

def

ghi

jkl

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).

Journal of Biogeography 34, 699–712 709 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd A. S. Paula, L. Diotaiuti and C. Galva˜ o geological history of the Neotropical region point to a number chains developed along the continental margin. However, the of vicariance events having caused the disjunction patterns Eastern Cordillera was formed as a result of the interaction observed today (Fig. 2). Most events were associated with between the Paleogene Caribbean thrusting and Neogene tectonic movements and inundations, with long-term and tectonic inversion during Andean compression. These struc- local dispersions also having some impact. tures were greatly affected by a complex system of strike–slip A general pattern shows a separation between Caribbean– faults and folds. We think that the break-up of the Andes into Antillean elements from a continental Neotropical component, three separate cordilleras was a geological event leading to the followed by a division between the south-east Amazonia– evolution of R. colombiensis, R. brethesi and R. neivai within Atlantic Forest and north-west South America–Central Amer- their respective geographical ranges. ica components (Fig. 2). Other, more regional events follow. The major geological events believed to have occurred at the There is evidence of repeated inundation of the Neotropical intersection of South, Central and North America are region that may have resulted in vicariance events in the described by Hallam (1994). In the Jurassic, North and South Cretaceous as well as the Eocene, Miocene and Pleistocene America were joined and Central America as we know it today epochs of the Quaternary period (Amorim, in press). did not exist. In the early Cretaceous, North and South Amorim & Pires (1996) and Amorim (2001, in press) America separated just to the south of the Yucatan peninsula. showed many more endemic areas in the Neotropical region, Volcanic islands subsequently appeared in the gap between but lacked information to reconstruct their histories. Accord- southern Mexico and Colombia. These were pushed north- ing to these authors, additional studies are needed to add new eastwards by the Farallon Plate, which in the mid-Cretaceous areas of endemism; subdivide some existing areas into smaller began to form Cuba, the Greater Antilles and the islands off the units (e.g. AnMA, SWAm); and establish a sequence for area Venezuelan coast. By the early Oligocene, another archipelago components that can be subdivided into polytomies (as for had been created between South and North America, the SWAm). widest gap between islands being in the Panama region. The Although the Neotropical region may conveniently be land corridor between South and North America was com- considered as a single biogeographical unit, it is geologically pleted in the Pliocene with the emergence of the Isthmus of complex. The Neotropics include not only the South American Panama and north-west Colombia. Rhodnius pallescens occurs continental plate, but also the southern portion of the North only in Central America and could only have speciated after American and Caribbean plates (Clapperton, 1993). The the isthmus was formed. complicated geological history of the region, in which these The Serra do Mar and Serra da Mantiqueira mountain plates intermittently separated and collided throughout the systems are younger than the Andes, having formed between Cretaceous and the Tertiary, provides the milieu within which the Oligocene and Pleistocene (Amorim & Pires, 1996). The interactions between organisms have occurred. South America results of our study indicate that many duplication events has been an island continent for most of the evolutionary (speciations within an area) occurred in AtlFor. As these events history of some organisms (e.g. angiosperms), whereas Central are usually allopatric and associated with a local or temporary America constitutes one of the two tropical parts of the dispersal barrier within an area, the uplift of the Serra do Mar Laurasian ‘supercontinent’. The outstanding geological feature and Serra da Mantiqueira could have resulted in the speciation of South America is the Andes, the longest mountain range in of R. domesticus, P. tertius, P. coreodes and R. nasutus. Uplift the world. Andean tectonic history is extremely important in of these mountains may also explain the origin and dispersal of understanding biogeographical process and pattern. It is now R. prolixus and R. robustus from AtlFor. known that the Andes were built by compressional tectonics Pinho et al. (1998) collected R. prolixus in Atlantic rain during the last 90 Myr or even longer. It is, therefore, overly forest near Tereso´polis, in the Serra do Mar. The specimens simplistic to view Andean vicariance as a singular event (adults, nymphs and eggs) were found in the axils of occurring with the Miocene uplift (Lundberg et al., 1998). Pteridophyta leaves, in foliage and on the trunks of palm The Andes essentially represent a classical tectonic upthrust trees. This was the first report of Rhodnius colonizing of continental rock, the result of a collision between the Pteridophyta, and some researchers have suggested that these leading edge of the westward-moving South American and insects were descended from escaped laboratory-bred speci- oceanic Pacific Plates (Lundberg et al., 1998). The southern mens. Based on previous studies and our own findings (Fig. 9), Andes are the oldest, with significant uplift already present in R. prolixus could have speciated in the Atlantic Forest of the the early Cenozoic, prior to the Oligocene. Most of the uplift of Serra do Mar, following dispersal to north-west South America the Central Andes was in the Miocene or later, whereas that and Central America. The distribution of this species in the of the northern portion of the range was mostly Plio- Serra do Mar should be studied further as it is the main target Pleistocene (van der Hammen, 1974). Rhodnius ecuadoriensis of Chagas’ disease vector control initiatives. could have speciated following the Central Andean uplift. As they extend northwards the Andes become more CONCLUSIONS geologically complex, breaking into three separate cordilleras (Aleman & Ramos, 2000). The Western and Central Cordil- The Rhodniini have a complex biogeographical history that leras of the Andes are typical subduction-related mountain has involved vicariance, duplications (sympatry), dispersal and

710 Journal of Biogeography 34, 699–712 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd Systematics and biogeography of Rhodniini extinction events. The main geological events affecting the Be´renger, J.M. & Pluot-Sigwalt, D. (2002) Rhodnius amazoni- origin and diversification of the Rhodniini in the Neotropics cus Almeida, Santos & Sposina 1973, bona species, close to were: (1) uplift of the Central Andes in the Miocene or later, R. pictipes Sta˚l, 1872 (Heteroptera, Reduviidae, Triatomi- (2) break-up of the Andes into three separate cordilleras nae). Memo´rias do Instituto Oswaldo Cruz, 97, 73–77. (Eastern, Central and Western) in the Plio-Pleistocene, (3) Brown, K.S., Jr (1979) Ecologia geogra´fica e evoluc¸a˜o nas flor- formation of a land corridor connecting South and North estas neotropicais. Universidade Estadual de Campinas, America in the Pliocene, and (4) uplift of the Serra do Mar and Campinas, Brazil. Serra da Mantiqueira mountain systems between the Oligocene Charleston, M.A. (1998) Jungles: a new solution to the host/ and Pleistocene. The relationships and biogeographical history parasite phylogeny reconciliation problem. Mathematical of the species of Rhodniini to the Neotropical region probably Biosciences, 149, 191–223. arose from the areas of endemism proposed by Amorim (2001, Charleston, M.A. & Page, R.D.M. (2001) TreeMap for Macin- in press). tosh. Version 2.0. http://taxonomy.zoology.gla.ac.uk/rod/ treemap.html Clapperton, C.M. (1993) Quaternary geology and geomorphol- ACKNOWLEDGEMENTS ogy of South America. Elsevier, Amsterdam. We thank Dr Carl Schaefer (University of Connecticut) and Cox, C.B. & Moore, D. (2005) Biogeography: an ecological and Dr Thomas Henry (Smithsonian Institution) for comments evolutionary approach, 7th edn. Blackwell Publishing, on an early version of the manuscript. Dr Dalton de Souza Oxford, UK. Amorim (Faculdade de Filosofia, Cieˆncias e Letras de Ribeira˜o Cracraft, J. (1994) Species diversity, biogeography, and the Preto/USP) provided us with figures from his studies (Figs 1 evolution of biotas. American Zoologist, 34, 33–47. & 2). Dr Gustavo Graciolli (Universidade Federal de Mato Galva˜o, C., Carcavallo, R.U., Rocha, D.S. & Jurberg, J. (2003) A Grosso do Sul) commented on the TreeMap results. Dr Malte checklist of the current valid species of the subfamily Tria- C. Ebach, Dr Juan J. Morrone and Dr John Grehan made tominae Jeannel, 1919 (Hemiptera, Reduviidae) and their constructive criticisms in reviewing our manuscript. Dr Bruce geographical distribution, with nomenclatural and taxo- Alexander (Liverpool School of Tropical Medicine) made the nomic notes. Zootaxa, 202, 1–36. English revision and provided comments that improved our Hallam, A. (1994) An outline of Phanerozoic biogeography. manuscript. The study was supported by grants from the Oxford Biogeography Series No. 10. Oxford University Centro de Pesquisas Rene´ Rachou/FIOCRUZ, Fundac¸a˜ode Press, Oxford, UK. Amparo a Pesquisa de Minas Gerais (FAPEMIG), and van der Hammen, T. (1974) The Pleistocene changes of Conselho Nacional de Desenvolvimento Cientı´fico e Tec- vegetation in tropical South America. Journal of Biogeogra- nolo´gico (CNPq). phy, 1, 3–26. Harold, A.S. & Mooi, R.D. (1994) Areas of endemism: defi- nition and recognition criteria. Systematic Biology, 43, 261– REFERENCES 266. Aleman, A. & Ramos, V.A. (2000) Northern Andes. Tectonic Hausdorf, B. (2002) Units in biogeography. Systematic Biology, evolution of South America (ed. by U.G. Cordani, E.J. Milani, 51, 648–652. A. Thomaz Filho and D.A. Campos), pp. 453–480. 31st Humphries, C.J. & Ebach, M. (2004) Biogeography on a International Geological Congress, CPRM/SGB, Rio de dynamic Earth. 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Lent, H. & Wygodzinsky, P. (1979) Revision of the Triato- Sanderson, M.J. & Shaffer, H.B. (2002) Troubleshooting mo- minae (Hemiptera, Reduviidae) and their significance as lecular phylogenetic analysis. Annual Review of Ecology and vectors of Chagas disease. Bulletin of the American Museum Systematics, 23, 49–72. of Natural History, 163, 123–520. Sanmartı´n, I. & Ronquist, F. (2004) Southern Hemisphere Lent, H., Jurberg, J. & Galva˜o, C. (1993) Rhodnius stali n. sp., biogeography inferred by event-based models: plant versus afim de Rhodnius pictipes Sta˚l, 1872 (Hemiptera, Reduviidae, animal patterns. Systematic Biology, 53, 216–243. Triatominae). Memo´rias do Instituto Oswaldo Cruz, 88, 605– Schaefer, C.W. (2005) Why are the subfamily relationships of 614. Triatominae (Hemiptera: Reduviidae) important? Entomo- Lundberg, J.G., Marshall, L.G., Guerrero, J., Horton, B., Mala- logı´a y Vectores, 12, 19–35. barba, C.S.L. & Wesslingh, F. 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(1969) ´Indice dos topoˆnimos York, USA. contidos na Carta do Brasil 1:1000000 do IBGE. FAPESP, Sa˜o Nihei, S.S. & Carvalho, C.J.B. (2004) Taxonomy, cladistics and Paulo. biogeography of Coenosopsia Malloch (Diptera, Antho- Zink, R.M., Blackwell–Rago, R.C. & Ronquist, F. (2000) The myiidae) and its significance to the evolution of anthomyiids shifting roles of dispersal and vicariance in biogeography. in the Neotropics. Systematic Entomology, 29, 260–275. Proceedings of the Royal Society of London Series B, Biological Page, R.D.M. & Charleston, M.A. (1998) Trees within trees: Sciences, 267, 497–503. phylogeny and historical associations. Trends in Ecology and Evolution, 13, 356–359. Page, R.D.M. & Homes, E.C. (1998) Molecular evolution: a phylogenetic approach. Blackwell Science, Oxford, UK. BIOSKETCHES Paula, A.S., Diotaiuti, L. & Schofield, C.J. (2005) Testing the sister-group relationships of the Rhodniini and Triato- Alexandre Silva de Paula has a DS in Entomology from mini (Insecta: Hemiptera: Reduviidae: Triatominae). Mole- Universidade Federal de Vic¸osa, Brazil. His research focuses on cular Phylogenetics and Evolution, 35, 712–718. the systematics and biogeography of Triatominae. He teaches Pinho, A.P., Gonc¸alves, T.C.M., Russell, N.S. & Cansen, A.M. Systematics at Centro de Pesquisas Rene´ Rachou/FIOCRUZ. (1998) The occurrence of Rhodnius prolixus Sta˚l, 1859, infected by Trypanosoma cruzi in the state of Rio de Janeiro, Lile´ ia Diotaiuti has a DS in Parasitology from Universidade Brazil (Hemiptera, Reduviidae, Triatominae). Memo´rias do Federal de Minas Gerais, Brazil. Her research focuses on Instituto Oswaldo Cruz, 93, 14–143. Chagas disease vectors control in Latin America. She teaches Platnick, N.I. (1991) Commentary. Areas of endemism. Aus- Biology and Control of Triatominae, and Scientific Methodo- tralian Systematic Botany, 4, xi–xii. logy at Centro de Pesquisas Rene´ Rachou/FIOCRUZ. Ramos, V.A. & Aleman, A. (2000) Tectonic evolution of the Cleber Galva˜ o has a DS in Veterinary Science from Andes. Tectonic evolution of South America (ed. by U.G. Universidade Federal Rural do Rio de Janeiro, Brazil. His Cordani, E.J. Milani, A. Thomaz Filho and D.A. Campos), research focuses on biology, systematics and comparative pp. 635–685. 31st International Geological Congress, morphology of Triatominae. He teaches Medical Entomology CPRM/SGB, Rio de Janeiro. and Protozoology at Instituto Oswaldo Cruz/FIOCRUZ. Ronquist, F. (1997) Dispersal–vicariance analysis: a new approach to the quantification of historical biogeography. Systematic Biology, 43, 195–203. Editor: Malte C. Ebach

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