Biogeography and evolution of Amazonian triatomines (Heteroptera: Reduviidae): implications for Chagas disease surveillance in humid forest ecoregions

Biogeography and evolution of Amazonian triatomines (Heteroptera: Reduviidae): implications for Chagas disease surveillance in humid forest ecoregions

Fernando Abad-FranchI, II, ⁺; Fernando A Monteiro^III

^IInstituto Leônidas & Maria Deane-Fiocruz Amazônia, Rua Teresina 476, 69057-070 Manaus, AM, Brasil

^IIPMBU-ITD, London School of Hygiene and Tropical Medicine, London, UK

^IIIInstituto Oswaldo Cruz-Fiocruz, Rio de Janeiro, RJ, Brasil

ABSTRACT

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

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

AMAZONIA

The Amazon is the largest subregion within the Neotropical biogeographical region. It encompasses 13 biogeographical provinces and over 40 ecoregions (cf. Olson et al. 2001, WWF 2001, Morrone 2006) (Tables I-III, Fig. 1). The greater Amazon biome (~ 6.5 million km²) is comprised of many diverse biotic communities. The Amazon River fluvial network, with over 10 thousand tributaries, irrigates > 5 million km² of tropical forests (moist and dry, terra firme and seasonally flooded, lowland and montane) and the open formations, Campinas, Campinaranas, and anthropic landscapes that constitute the ecological mosaic of Amazonia. Considered as a whole, the Amazon is the most biologically diverse biome on Earth as measured by the absolute number of species recorded in each region (Mittermeier et al. 2003).

From a wider (biogeographical, ecological, and evolutionary) perspective, the Amazon complex may be considered to include certain physically contiguous systems and ecoregions with which it shares key aspects of its historical biogeography. The most important among these regions are the Orinoco and Tocantins/Araguaia basins, the Guyanan Shield highlands, and the eastern slopes of the northern-central Andes (including the Peruvian Selva Alta, the Yungas, and the inter-Andean valleys draining towards the Amazon-Orinoco system). In Brazil, both the drier ecoregions of the Cerrado and the Caatinga (particularly the relatively humid forests along riverbanks and mountain ranges) and the moist Atlantic Forests harbour animal and plant communities that reveal their ancient biogeographical-evolutionary relationship with Amazonia.

Many factors and processes have been invoked to explain the regional patterns of biological diversification. Whatever the weight of their relative contributions, geological substrate heterogeneity, climatic fluctuations and habitat fragmentation, hydro- and oro-graphical vicariant events, dispersal and adaptive radiation, local extinction, genetic drift or coevolution all have probably played a role. It seems safe enough to admit that the historical evolution of this huge biogeographical complex offered a vast number of ecological-adaptive opportunities (and constraints) for organic diversification by natural selection of variants, thus shaping the systematic relationships among contemporary lineages (cf. Rossetti et al. 2005). It is therefore obvious that a sound understanding of the biology of Amazonian organisms must take into account not only their systematic structuring and current ecological associations, but also the historical (evolutionary) aspects of the different lineages and of the environments where they originated and diversified.

THE TRIATOMINAE OF AMAZONIA

The true number of Amazonian triatomine species remains probably unknown. Records from the Amazon-Orinoco-Tocantins/Araguaia systems, the Guyana Shield, and the eastern Andean foothills include no less than 27 recognised species (with a few further taxa probably present in some subregions) grouped into nine genera and five tribes: Rhodniini (ten Rhodnius and at least one Psammolestes species), Triatomini (four Triatoma, three Panstrongylus, and two Eratyrus species) Caverni-colini (two Cavernicola species), Alberproseniini (two Alberprosenia species), and Bolboderini (at least two Belminus and one Microtriatoma species) (see Tables II, ^III). It is however very likely that many further taxa occur in the Amazon that have not yet been formally described. Lineages composed of small, dull-coloured, canopy-living organisms (like those within the last three tribes we have just mentioned) are the most obvious candidates to encompass undescribed species. Other likely candidates are those 'species' considered to be either biologically very variable and/or extensively distributed, which might conceal species complexes. The recent finding of moderately divergent mitochondrial haplotypes in phenotypically indistinguishable populations of the widespread R. robustus (Monteiro et al. 2003) indicates that the biological diversity of well-known triatomine taxa is also higher than previously thought. The growing use of DNA barcoding techniques in arthropod taxonomy is revealing how underestimated is species richness in biodiversity inventories based on classical phenotypic approaches (see for instance Miller 2007).

Even a superficial biogeographical appraisal suggests that the many triatomine species reported to occur in Amazonia fall into distinct categories. Some must be considered as truly Amazonian, while others evolved elsewhere and occupied the region secondarily. Among the former, some radiated to neighbouring ecoregions and diversified (speciating in some cases), while others remained endemic to their areas of origin. Among the latter, some are populations of widely distributed species, others are found in the ecotones along the fringes of the region, and a few represent isolated populations derived from currently allopatric stem lineages.

In an attempt to put forward a coherent account of the systematic, ecological, and behavioural diversity of Amazonian triatomines, we underscore in this paper the importance of adopting a biogeographical and evolutionary stance – which might be broadly interpreted as phylogeographical. Following this rationale, we present an approximation to the historical biogeography and evolution of the main triatomine lineages known to occur in the greater Amazon, classifying them accordingly, and discuss how this view may foster a biologically sound understanding of synanthropic behavioural trends among these vectors.

A PHYLOGEOGRAPHICAL CLASSIFICATION OF AMAZONIAN TRIATOMINES

The draft classification we propose here is based on an approximation to the evolutionary origins and diversification patterns of the Amazonian lineages within the Rhodniini, Panstrongylus and Triatoma, but we will also consider other groups. The judgments underlying our proposal are biogeographical, ecological, and evolutionary; we made an effort to avoid excess speculation by trying to focus on taxon groups that can be safely considered to be monophyletic, even if they are not recognised as formal systematic units in some cases.

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

The paradigmatic example of this group is the tribe Rhodniini, an assemblage of arboricolous triatomines (most of them associated with palm trees) grouped into two genera – Psammolestes and Rhodnius (Lent & Wygodzinsky 1979, Galvão et al. 2003). While the phylogenetic relationships of many triatomine tribes and genera remain problematic, the Rhodniini are considered monophyletic beyond controversy (Hypša et al. 2002, De Paula et al. 2005). The two genera within the tribe are however paraphyletic, with Psammolestes species sharing a common ancestor with R. robustus and its closest relatives (Monteiro et al. 2000, 2002).

The 19 species within the tribe Rhodniini have been classified into two main groups (Schofield & Dujardin 1999). The 'pictipes group' includes species from both the eastern (pictipes, stali, brethesi, paraensis, and amazonicus) and western (pallescens, colombiensis, and ecuadoriensis) sides of the Andes. The members of the 'robustus group' (robustus, prolixus, nasutus, neglectus, milesi, dalessandroi, domesticus, and the Psammolestes) are all cis-Andean [only R. neivai, endemic to the dry forests of the eastern Maracaibo biogeographical province, includes geographically restricted trans-Andean populations]. However, the very presence of two biogeographically well-defined groups of species (cis- and trans-Andean) has also been interpreted as signalling a basal evolutionary split within the tribe. Mitochondrial rDNA sequence analyses failed to provide convincing evidence to uphold any of these two competing hypotheses (Hypša et al. 2001, De Paula et al. 2007), but mt cytochrome b gene (cytb) genealogies tend to support the existence of two major, monophyletic groups: the 'pictipes' and the 'robustus' lineages (Abad-Franch & Monteiro 2005 and unpublished data).

Several lines of evidence suggest a palaeo-Amazonian origin of the Rhodniini. First, only three of the known extant species are entirely trans-Andean (see above). Eleven of the 16 cis-Andean species have been recorded in the greater Amazon (including the Orinoco and Tocantins/Araguaia systems); the best studied among these (particularly R. robustus) are genetically very diverse entities probably encompassing several, recently diversified cryptic taxa (Monteiro et al. 2003). These data suggest that the core biogeographical region of the tribe would correspond to contemporary Amazonia. The close ecological association between most Rhodnius species and palm trees may reflect a long (perhaps up to > 90 million years) process of parallel evolution of both lineages (Gaunt & Miles 2002). Palm trees first evolved in moist tropical forests of the Gondwana floral province during the warm late Cretaceous, and occupied drier life zones secondarily (cf. Cox & Moore 2000). Assuming that the Rhodniini followed their palm ecotopes along this evolutionary pathway, it may be concluded that they also appeared for the first time in humid tropical forests. The exclusively Neotropical range of extant lineages suggests that they probably evolved in the moist Equatorial forests of western Gondwana. The average cytb sequence divergences between the more widely distributed representatives of the tribe (R. pictipes and R. robustus) exceeds 20% (FA-F & FAM, unpublished data), suggesting that their most recent common ancestor lived in the Miocene [10-12 million years ago (Mya); assuming a rate of 2.3% pairwise sequence divergence per million years (Brower 1994)], when flooded moist forests (similar to contemporary várzea) prevailed in the Amazon (cf. Hoorn 1994).

The diversification of these palaeo-Amazonian ancestors followed diverse patterns. Mt cytb sequence data suggest that R. pictipes and R. pallescens-colombiensis share a common ancestor that lived in the late Miocene (~ 6 Mya), just before the Andes increased their maximum altitude to over 4000m (Cox & Moore 2000, Abad-Franch et al. 2003). The time since divergence of R. ecuadoriensis from its Colombian relatives (R. pallescens and R. colombiensis) (~ 5 Mya) roughly coincides with the uplift of the Andes in the Pliocene. A plausible explanation to the current distribution of the members of the Pacific Rhodnius lineage would therefore combine the effects of adaptive radiation and vicariance. An ancestral population perhaps reached the western side of the (then low) Andes range during the late Miocene by migrating from the eastern Orinoco plains; subsequently, the rise of the Andes during the Pliocene split that population into two main clades: the northern (now Colombian) cluster, comprising the ancestral forms of R. pallescens and R. colombiensis, and an isolated pocket in the south, which adapted to new ecotopes and eventually gave rise to R. ecuadoriensis (Abad-Franch et al. 2003).

The bulk of the diversification of the Amazonian Rhodnius lineages (the cis-Andean group derived from the 'pictipes lineage' and all the known representatives of the 'robustus lineage') probably took place in synchrony with the orographic-hydrographic changes and the climatic fluctuations (with profound local and regional ecological impact) that took place in the late Pliocene and the Pleistocene (cf. Rossetti et al. 2005). During interglacial periods for instance, moist forests expanded beyond their current limits, allowing for the colonisation of new regions by representatives of the tribe. Some of them dispersed towards presently arid or semi-arid ecoregions, particularly the Colombian-Venezuelan Llanos to the north and the Brazilian Cerrado and Caatinga to the south. In some cases, these ancestral dispersing populations established ecological associations with dry forest palm species (Copernicia tectorum-R. prolixus, C. prunifera-R. nasutus, Acrocomia spp.-R. neglectus), while in others they reached new territories following Mauritia flexuosa gallery forests or adapting to protected microenvironments (Psammolestes-bird nests). The genetic consequences of Amazonian moist forest fragmentation during the Pleistocene can be traced in the relationships between R. robustus mt cytb haplotypes, with at least four moderately distinct variants (~ 2.3-4% sequence divergence) occurring across the greater Amazon (Monteiro et al. 2003, Abad-Franch & Monteiro 2005; see Fig. 2). The phylogeographic hypothesis proposed by Monteiro et al. (2003) to explain the diversification of these Amazonian R. robustus clades would receive further support if R. pictipes populations (with similar overall geographic distribution) were shown to present comparable patterns of genetic structuring. The question has not been thoroughly examined so far.

R. domesticus is probably the living representative of an ancient coastal lineage that remained isolated from its Amazon ancestors when the humid forest corridors linking Amazonia with the Brazilian Atlantic Forest disappeared. A similar process of early isolation might have given rise to R. neivai in the northern xeric forests and shrublands of the Maracaibo biogeographical province.

The apparent ecological specialisation of some Rhodnius and Psammolestes species may have also played a role in the diversification of the tribe. Thus, R. brethesi seems to be tightly associated with Leopoldinia piassaba palms, and it has been suggested that the distribution of R. stali closely matches that of Attalea phalerata palms in the southwestern fringe of the Amazon biome (Matías et al. 2003). R. paraensis is thought to be associated with an arboreal rodent of the genus Chrysurus, and a similar process of host specialisation, in this case involving birds (mainly Furnariidae), may have resulted in the diversification of the Psammolestes from an ancestral form belonging to the 'robustus lineage'.

Some less well-studied triatomine taxa also appear to have evolved in the Amazon moist forests. These include the Cavernicolini, the genus Eratyrus, Microtriatoma trinidadensis, and perhaps the Belminus-Parabelminus lineage. The phylogenetic affinities and evolutionary origins of these groups have not been thoroughly investigated; our statements about them, based on ecological-biogeographic information, are therefore only tentative. The two known Cavernicola species live in close association with cave- and hollow tree-dwelling bat colonies (Barrett 1991). C. pilosa is a widely distributed species; while records exist from several extra-Amazonian ecoregions, the core of its distribution lies apparently within Amazonia. C. lenti has only been reported to occur in a geographically restricted area within the Uatumã-Trombetas moist forests of the Brazilian Amazon. These data suggest an Amazonian origin of the tribe, followed by passive, host-mediated spread of the pilosa lineage. E. mucronatus occurs in hollow trees throughout the Amazon-Orinoco basins, whereas cis-Andean E. cuspidatus populations seem restricted to Northern Venezuela, also suggesting an Amazonian common ancestor of the genus. The biogeographical pattern of M. trinidadensis (which occurs in a ring encompassing the Amazon-Orinoco fringes) could be interpreted as the result of a centrifugal adaptive radiation of populations of Amazonian origin. A prediction of this hypothesis is that the species should be present in central Amazonia, but no records existed from the area (Carcavallo et al. 1999, Galvão et al. 2003) until the recent collection of a male specimen in the Japurá/Solimões-Negro moist forests (Brazilian central Amazon) (FA-F, unpublished). The Belminus-Parabelminus lineage has also several representatives in the Amazonas-Orinoco system, but some species are trans-Andean and some (the Parabelminus) are endemic to the Brazilian Atlantic Forests; it is therefore difficult to put forward a hypothesis about its origins, and they could well fit also in the second subdivision of our classification.

Widely distributed lineages - Several triatomine species reported from the greater Amazon belong to widely distributed lineages whose centre of origin and diversification lies outside the region. They probably occupied Amazonian ecoregions secondarily; while some were awarded formal specific status, others are simply considered geographical populations of their parental species. Representatives of this second major class all belong to the genus Panstrongylus, but the Belminus-Parabelminus lineage could have followed similar evolutionary pathways.

Amazonian Panstrongylus populations belong to three species (P. geniculatus, P. lignarius-herreri, and P. rufotuberculatus) that seem to be related to the Mesoamerican Triatomini lineage (Marcilla et al. 2002). The ancestors of this lineage evolved several million years before the complete closure of the Panama Isthmus, ~ 3 Mya (Bargues et al. 2000, Cox & Moore 2000), suggesting a secondary occupation of South America by their descendants. P. geniculatus is a widely distributed and phenotypically diverse triatomine species. It survives in arid life zones by exploiting highly protected, humid underground microhabitats (particularly armadillo burrows). This strategy probably helped it disperse towards the Amazon across the dry regions of northern South America. Once in the moist Amazon forests, P. geniculatus colonised less protected environments such as hollow trees, dead logs, palm tree crowns, and, sporadically, peridomestic pigsties. P. lignarius belongs to a small monophyletic group of arboricolous species that occupy moist tropical forests in Central America (P. humeralis) and the Amazon (P. lignarius). A synanthropic population (P. herreri, recently synonymised with lignarius) lives in the dry forests of the Marañón valley in Northeastern Peru. It probably represents a parapatric derivative of lowland Amazonian populations known as P. lignarius. Sporadic records suggest that P. rufotuberculatus is also present throughout the greater Amazon. Its extensive geographic range, its phylogenetic affinities with Mesoamerican Triatomini, and its ecological plasticity all suggest a secondary spread of this species across Amazonian ecoregions.

Relict species: the strange case of T. maculata - T. maculata is the only representative of the genus Triatoma with abundant native populations within the greater Amazon. It is probably also the only representative of the biogeographically South American Triatoma lineage that occurs north of the parallel 10 ºS. Its presumed sister species (T. pseudomaculata) and its closest relatives (T. wygodzinskyi and T. arthurneivai) occur in the Caatinga and the Cerrado. The vicariant distribution of these species in dry ecoregions north and south of the moist Amazon forests was interpreted as the result of passive dispersal of nymphs by migratory birds. This hypothesis seems to have been refuted by recent allozyme data showing large genetic distances separating T. maculata from T. pseudomaculata (as opposed to the very small differences detected between the latter and T. wygodzinskyi; dos Santos et al. 2007). These results are compatible with a complex phylogeographic scenario in which an ancestral Triatoma population occupied dry corridors linking the arid Brazilian Northeast region with the savannahs of the Orinoco system. The ancestors of extant T. maculata populations became isolated from their southern relatives when the moist tropical forest matrix closed those dry corridors, setting out the process of independent evolution we can now trace with genetic markers. The diversification of the southern lineage is reflected in the several species that have been formally described, while the northern clade is still considered monospecific (comprising only T. maculata). A thorough assessment of the genetic and phenotypic variability within T. maculata may therefore be predicted to reveal much more diversity than would be expected among populations of a recently dispersed species. In summary, contemporary T. maculata populations probably represent an old relict from the times when tropical dry forest corridors traversed Amazonia from north to south.

In the fringes of the Amazon - A few populations of primarily Andean triatomine species have been recorded in montane foothill forests that belong to the greater Amazon biome. This is the case of T. carrioni in Ecuador (where T. venosa also occurs) and Northern Peru (Abad-Franch et al. 2001, Cuba Cuba et al. 2002). T. nigromaculata also belongs to the carrioni-venosa-dispar lineage, and is therefore probably of Andean origin. Its range includes a large portion of the Venezuelan Orinoco and coastal basins and the Guyanan highlands, where it preferentially occurs in dry ecoregions. P. chinai and R. ecuadoriensis, both primarily trans-Andean, occur in the upper (Andean) stretches of some Peruvian valleys that drain into the Amazon. R. colombiensis, occasionally included in checklists of Amazonian triatomines, is endemic to the Magdalena Valley dry forests, and therefore exclusively trans-Andean. Records of T. sordida and T. infestans in the Bolivian Amazon may be the result of mislabelling or may represent passively dispersed individuals carried beyond their natural biogeographic range. All the species in this class, perhaps with the exception of T. nigromaculata, seem however to have limited tolerance to the general ecological conditions of the core Amazon region, and may therefore be predicted to remain confined to relatively small, peripheral areas.

Artificial introductions - T. rubrofasciata is a tropicopolitan species that occupies artificial environments in harbour cities, generally in association with rats. Its presence in Belém or São Luís, the main sea harbours of the Brazilian Amazon region, is therefore hardly surprising. The most likely explanation, given the phylogenetic affinities, geographical range, and habits of this species, is that Amazonian populations were introduced by sea trade into the region. Domestic populations of other, more dangerous species are also candidates to artificial introduction.

Particularly worrying is the case of R. prolixus, now the main vector of human Chagas disease, which is native to the drier forests of the Orinoco basin system (mainly the Llanos) but may also colonise humid environments. There are sparse records of this species in several Amazonian localities (in Brazil, the Guyanas, and Colombia), and the southern limits of sylvatic R. prolixus populations have not been defined so far. Their capacity to adapt to palm tree genera with wide distribution throughout Amazonia (such as Attalea) is well documented, and may signal a potential for southward dispersal. In the Venezuelan-Colombian Llanos, sylvatic R. prolixus from Attalea palms contribute to the infestation and reinfestation of houses and peridomestic structures. Finally, preliminary mt cytb data have revealed the existence of a third cryptic taxon within the monophyletic group composed of R. prolixus and R. robustus I (sensu Monteiro et al. 2003). It occurs in Attalea palms of the central Brazilian Amazon (FAM & FA-F, unpublished data). The presence of these genotypes in Amazonian moist forests configures a potentially dangerous situation that should be carefully monitored. Introduced T. infestans populations reached the southeastern limits of the Brazilian Amazon, but were subsequently eliminated. In northeastern Bolivia, some of the regions where sylvatic populations are common include inter-Andean valleys that drain into the Amazon. Both empirical field data and eco-geographical models (Gorla 2002) suggest however that T. infestans has a limited ability to thrive in the warm and humid climate conditions of most Amazonian forest regions. T. dimidiata natural populations are on the contrary present in many, extremely diverse ecoregions (from the Yucatán Peninsula to Ecuador), including both dry and moist forest environments, and could perhaps colonise artificial structures in the Amazon.

THE ECOLOGICAL AND EVOLUTIONARY CONTEXT OF SYNANTHROPIC TRENDS IN AMAZONIAN TRIATOMINES

Amazonian triatomines are essentially sylvatic. Epidemiological and entomological data suggest however that sporadic contact between Trypanosoma cruzi-infected vectors and humans, even if relatively infrequent, occurs throughout the region. Most cases of T. cruzi transmission to humans are mediated by adult triatomines that invade houses, attack forest workers or contaminate food-processing equipment (see Aguilar et al. 2007, this volume). On the other hand, several native triatomine species colonise artificial environments in well-defined micro-regions. These different degrees of synanthropism may be interpreted as a behavioural gradient starting with the mere invasion of a house by an adult adventitious bug and eventually leading to the stable infestation of human dwellings by large breeding vector colonies. Understanding the relative roles of ecological and evolutionary factors in the shaping of this gradient may substantially improve our ability to predict which species are likely to progress along the gradient, and may also help identify weak (and strong) links that could (or could not) be used as the targets of disease prevention strategies. We now present a tentative partition of such ecological and evolutionary components based on our overview of the historical biogeography of Amazonian triatomines.

Ecological factors - Random events and ecological pressure linked to anthropic landscape transformation are probably key factors in the initial portion of the behavioural gradient leading to synanthropism. The dynamics of land occupation in the Amazon moist forest ecoregions illustrate particularly well this process. Initially, forest clearance leads to a reduction of wild vertebrate populations; a pattern of selective deforestation in which palm trees are kept in peridomestic environments is commonplace. Palm triatomine populations (mainly Rhodnius species) are probably subject to high mortality during this phase, but do not disappear completely. The palms become suitable shelters for opportunistic marsupials and rodents (Didelphis marsupialis, Rattus spp.) that proliferate in human-modified environments. Residual triatomine populations may take advantage of this situation, using these (now abundant) blood sources to recover and eventually build-up large colonies in some palms (Abad-Franch et al. 2005). When the system nears its carrying capacity, a reduced availability of blood per individual results in adult starved triatomines frequently flying into nearby houses. Humans, palms, adventitious triatomines and opportunistic mammals (often infected by T. cruzi) closely coexist in anthropic landscapes throughout the Amazon, increasing disease transmission risk (Aguilar et al. 2007, this volume).

However, it is evident that only a small fraction of the triatomines that reach human dwellings founds viable domestic breeding colonies. Most die off; a few may perhaps lie eggs, but their offspring only reach the reproductive stage on very rare occasions. It is conceivable that the (relatively few) triatomine populations with the capacity of thriving in artificial microenvironments may have acquired (through natural selection) some characteristics that distinguish them from others of the same lineage that cannot establish domestic colonies.

Evolutionary factors - Natural selection of any trait that could favour specifically the adaptation of a triatomine population to artificial ecotopes (built by humans) can only have operated during the last 10 to 12 thousand years, which is the approximate age of the first known human settlements in the Americas. Such an event seems extremely unlikely in the absence of a very strong and persistent directional selective pressure. We may envisage, however, that a set of traits exists that, having been selected over millions of years for other reasons, confers the ability to exploit domestic habitats to the populations that possess it. Populations of the same lineage lacking those traits would fail to permanently infest households. In such a case, we would expect that only a few populations among all the possible candidates within a given lineage (those that possess the set of traits in question) be able to successfully colonise artificial environments. The biogeographical-evolutionary scenario we have proposed here for the Rhodniini suggests that, at least for several lineages within the tribe, natural selection of variants adapted to relatively dry microclimates may be related with the progressing of some species (and not others) along the gradient of synanthropic behaviour.

Thus, all the populations of Rhodnius spp. that succeed in colonising artificial environments (mainly of R. prolixus, but also of R. neglectus, R. nasutus, R. stali, R. pallescens, and R. ecuadoriensis) derive from ancestral populations that adapted to arid or semi-arid climates long before human beings reached the Americas. Also within the Amazon, domestication foci (particularly of R. stali, but also of T. maculata or P. herreri) are located in the regions with lowest mean annual rainfall or longest rain-free periods (cf. Sombroek 2001). This pattern may in fact be even more general, affecting other humid forest triatomines; for instance, T. dimidiata populations seem to colonise human dwellings only out of the moist forests of the Yucatán-Petén region (Dorn et al. 2007). These observations suggest that species or populations of triatomines that evolved to breed in extremely humid microenvironments (such as Amazonian rainforest palm tree crowns) may have only a limited potential to successfully colonise artificial environments, perhaps as a consequence of low tolerance towards the slightly drier microclimate of human dwellings. A prediction of this hypothesis is that field-collected specimens from moist forest ecotopes would fail to thrive towards the drier end of an artificial humidity gradient in the laboratory. If confirmed, this pattern would signal a truly evolutionary component of the process of infestation and colonisation of human environments by triatomines. It could help us to identify differential risk areas by mapping widely available climate data, and perhaps, in the future, to determine the potential for domiciliation of vector species or populations on an individual basis.

CONCLUSIONS

The systematic, ecological, and behavioural patterns of any group of organisms are gradually whittled along the evolutionary history of the lineage, from the more or less ancient event at the origin of the clade to the contemporary phenomena that shape the genetic structuring of conspecific populations. One major consequence, as Dobzhansky (1973) observed, is that adopting an evolutionary perspective greatly widens our understanding of those patterns, opening new paths in the search for satisfactory (realistic) answers to old difficult questions from infectious disease control and surveillance to the mechanisms involved in the generation, maintenance and loss of biological diversity.

Equipped with ever more sophisticated analytical tools (morphometrics, molecular markers, environmental data obtained by remote sensors onboard artificial satellites, radiocarbon dating) we can face the challenge of adopting this evolutionary stance in our research on Chagas disease vectors, particularly when the questions refer to clearly monophyletic clades. Our review (provisional and incomplete) of the origin and diversification of Amazonian triatomines suggests research avenues that unfold in many directions, from the adequate understanding of the evolution of whole tribes over millions of years to the (probably necessary, and so far widely neglected) demarcation of the truly evolutionary and 'merely' ecological processes involved in the synanthropic behavioural gradient of the Triatominae.

Received 4 June 2007

Accepted 2 July 2007

Financial support: the UNDP-World Bank-WHO TDR Special Programme, Fiocruz, CNPq, Fapeam, the ECLAT Network. This paper is contribution no. 4 of the Research Programme on Infectious Disease Ecology in the Amazon (RP-IDEA) of the Instituto Leônidas & Maria Deane.

• Abad-Franch F, Monteiro FA 2005. Molecular research and the control of Chagas disease vectors. An Acad Bras Cienc 77: 437-454.
• Abad-Franch F, Monteiro FA, Patterson JS, Miles MA 2003. Phylogenetic relationships among members of the Pacific Rhodnius lineage (Hemiptera: Reduviidae: Triatominae). Infect Genet Evol 2: 244-245.
• Abad-Franch F, Palomeque FS, Aguilar VHM, Miles MA 2005. Field ecology of sylvatic Rhodnius populations (Heteroptera, Triatominae): risk factors for palm tree infestation in western Ecuador. Trop Med Intl Health 10: 1258-1266.
• Abad-Franch F, Paucar CA, Carpio CC, Cuba Cuba CA, Aguilar VHM, Miles MA 2001. Biogeography of Triatominae (Hemiptera: Reduviidae) in Ecuador: implications for the design of control strategies. Mem Inst Oswaldo Cruz 96: 611-620.
• Aguilar HM, Abad-Franch F, Dias JCP, Coura JR 2007. Chagas disease in the Amazon region. Mem Inst Oswaldo Cruz (this volume).
• Bargues MD, Marcilla JA, Ramsey J, Dujardin JP, Schofield CJ, Mas-Coma S 2000. Nuclear rDNA-based molecular clock of the evolution of Triatominae (Hemiptera: Reduviidae), vectors of Chagas disease. Mem Inst Oswaldo Cruz 95: 567-573.
• Barrett TV 1991. Advances in triatomine bug ecology in relation to Chagas disease. Adv Dis Vect Res 8: 143-176.
• Brower AVZ 1994. Rapid morphological radiation and convergence in the butterfly, Heliconius erato, inferred from patterns of mitochondrial DNA evolution. Proc Nat Acad Sci USA 91: 6491-6495.
• Carcavallo RU, Galíndez Girón I, Jurberg J, Lent H 1999. Atlas of Chagas Disease Vectors in the Americas, Vol. III, Fiocruz, Rio de Janeiro.
• Cox CB, Moore PD 2000. Biogeography. An Ecological and Evolutionary Approach Blackwell Science, Oxford.
• Cuba Cuba CA, Abad-Franch F, Roldán RJ, Vargas VF, Pollack VL, Miles MA 2002. The triatomines of northern Peru, with emphasis on the ecology and infection by trypanosomes of Rhodnius ecuadoriensis (Triatominae). Mem Inst Oswaldo Cruz 97: 175-183.
• de Paula AS, Diotaiuti L, Schofield CJ 2005. Testing the sister-group relationship of the Rhodniini and Triatomini (Insecta: Hemiptera: Reduviidae: Triatominae). Mol Phylogenet Evol 35: 712-718.
• de Paula AS, Diotaiuti L, Galvão C 2007. Systematics and biogeography of Rhodniini (Heteroptera: Reduviidae: Triatominae) based on 16S mitochondrial rDNA sequences J Biogeogr 34: 699-712.
• dos Santos CL, Lopes CM, Dujardin JP, Panzera F, Pérez R, Carbajal de la Fuente AL, Pacheco RS, Noireau F 2007. Evolutionary relationships based on genetic and phenetic characters between Triatoma maculata, Triatoma pseudomaculata and morphologically related species (Reduviidae: Triatominae). Infect Genet Evol doi:10.1016/j.meegid.2007.01.008.
• Dobzhansky T 1973. Nothing in biology makes sense except in the light of evolution. Am Biol Teacher 35: 125-129.
• Dorn PL, Monroy C, Curtis A 2007. Triatoma dimidiata (Latreille, 1811): A review of its diversity across its geographic range and the relationship among populations. Infect Genet Evol 7: 343-352.
• Galvão C, Carcavallo R, Rocha DS, Jurberg J 2003. A checklist of the current valid species of the subfamily Triatominae Jeannel, 1919 (Hemiptera, Reduviidae) and their geographical distribution, with nomenclatural and taxonomic notes. Zootaxa 202: 1-36.
• Gaunt MW, Miles MA 2002. An insect molecular clock dates the origin of the insects and accords with palaeontological and biogeographic landmarks. Mol Biol Evol 19: 748-761.
• Gorla D 2002. Variables ambientales registradas por sensores remotos como indicadores de la distribución geográfica de Triatoma infestans (Heteroptera: Reduviidae). Ecol Austral 12: 117-127.
• Hoorn C 1994. An environmental reconstruction of the palaeo-Amazon river system (middle-late Miocene, NW amazonia). Palaeo 112: 187-238.
• Hypa V, Tietz DF, Zrzavý J, Rego ROM, Galvão C, Jurberg J 2002. Phylogeny and biogeography of Triatominae (Hemiptera: Reduviidae): molecular evidence of a New World origin of the Asiatic clade. Mol Phylogenet Evol 23: 447-457.
• Lent H, Wygodzinsky P 1979. Revision of the Triatominae (Hemiptera: Reduviidae), and their significance as vectors of Chagas disease. Bull Am Mus Natural History 163: 123-520.
• Marcilla A, Bargues MD, Abad-Franch F, Panzera F, Carcavallo RU, Noireau F, Galvão C, Jurberg J, Miles MA, Dujardin JP, Mas-Coma S 2002. Nuclear rDNA ITS-2 sequences reveal polyphyly of Panstrongylus species (Hemiptera: Reduviidae: Triatominae), vectors of Trypanosoma cruzi Infect Genet Evol 1: 225-235.
• Marcilla A, Bargues MD, Ramsey JM, Magallón-Gastélum E, Salazar-Schettino PM, Abad-Franch F, Dujardin JP, Schofield CJ, Mas-Coma S 2001. The ITS-2 of the nuclear rDNA as a molecular marker for populations, species, and phylogenetic relationships in Triatominae (Hemiptera: Reduviidae), vectors of Chagas disease. Mol Phylogenet Evol< 18: 136-142.
• Matías A, de la Riva J, Martínez E, Torrez M, Dujardin JP 2003. Domiciliation process of Rhodnius stali (Hemiptera: Reduviidae) in Alto Beni, La Paz, Bolivia. Trop Med Intl Health 8: 264-268.
• Miller SE 2007. DNA barcoding and the renaissance of taxonomy. Proc Natl Acad Sci USA 104: 4775-4776.
• Mittermeier RA, Mittermeier CG, Brooks TM, Pilgrim JD, Konstant WR, da Fonseca GAB, Kormos C 2003. Wilderness and biodiversity conservation. Proc Natl Acad Sci USA 100: 10309-10313.
• Monteiro FA, Barrett TV, Fitzpatrick S, Cordón-Rosales C, Feliciangeli MD, Beard CB 2003. Molecular phylogeography of the Amazonian Chagas disease vectors Rhodnius prolixus and R. robustus Mol Ecol 12: 997-1006.
• Monteiro FA, Lazoski C, Noireau F, Solé-Cava AM 2002. Allozyme relationships among ten species of Rhodniini, showing paraphyly of Rhodnius including Psammolestes Med Vet Entomol 16: 83-90.
• Monteiro FA, Wesson DM, Dotson EM, Schofield CJ, Beard CB 2000. Phylogeny and molecular taxonomy of the Rhodniini derived from mitochondrial and nuclear DNA sequences. Am J Trop Med Hyg 62: 460-465.
• Morrone JJ 2006. Biogeographic areas and transition zones of Latin America and the Caribbean islands based on panbiogeographic and cladistic analyses of the entomofauna. Annu Rev Entomol 51: 467-494.
• Olson DM, Dinerstein E, Wikramanayake ED, Burgess ND, Powell GVN, Underwood EC, D'Amico JA, Itoua I, Strand HE, Morrison JC, Loucks CJ, Allnutt TF, Ricketts TH, Kura Y, Lamoreux JF, Wettengel WW, Hedao P, Kassem KR 2001. Terrestrial ecoregions of the World: a new map of life on Earth. Bioscience 51: 933-938.
• Pavan MG, Monteiro FA 2007. A multiplex PCR assay that separates Rhodnius prolixus from members of the Rhodnius robustus cryptic species complex (Hemiptera: Reduviidae). Trop Med Int Health 12: 751-758.
• Rossetti DF, de Toledo PM, Góes AM 2005. New geological framework for Western Amazonia (Brazil) and implications for biogeography and evolution. Quaternary Res 63: 78-89.
• Schofield CJ, Dujardin JP 1999. Theories on the evolution of Rhodnius Actual Biol (Medellín) 21: 183-197.
• Sombroek W 2001. Spatial and temporal patterns of Amazon rainfall. Consequences for the planning of agricultural occupation and the protection of primary forests. Ambio 30: 388-396.
• WWF-World Wildlife Fund 2001. Ecoregions of Latin America and the Caribbean. Available at http://www.conserveonline.org/docs/2001/06/lac_ecoregions.jpg

Publication Dates

• Publication in this collection
  21 Sept 2007
• Date of issue
  Oct 2007

History

• Accepted
  02 July 2007
• Received
  04 June 2007