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Systematics and Biogeography of Rhodniini (Heteroptera: Reduviidae: Triatominae)

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Systematics and Biogeography of Rhodniini (Heteroptera: Reduviidae: Triatominae) Journal of Biogeography (J. Biogeogr.) (2007) 34, 699–712 ORIGINAL Systematics and biogeography of ARTICLE Rhodniini (Heteroptera: Reduviidae: 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, Hemiptera, historical biogeography, Neotropical, Psammolestes, rDNA mitochondrial gene, Rhodnius, 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 insects 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 700 Journal of Biogeography 34, 699–712 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd Systematics and biogeography of Rhodniini Figure 1 Simplified picture of main areas of endemism for Neotropical organisms based on vertebrates,
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