NOTA RESEARCH NOTE 89 Biosystematics and evolution of the Triatominae Biossistemática e evolução de triatomíneos Christopher J. Schofield 1 1 London School of Hygiene Abstract In this paper we summarize the systematics of the 130 currently recognized species of and Tropical Medicine, Triatominae and the key features of their evolutionary background. There is increasing evidence London WC1 E7HT, UK [email protected] that the subfamily has polyphyletic origins, with the various tribes and species groups probably arising from different reduviid lineages in relatively recent times. Key words Triatominae; Classification; Evolution; Insect Vectors Resumo Neste trabalho resume-se a sistemática das 130 espécies de triatomíneos atualmente reconhecidas, com os elementos principais de sua evolução. Existem evidências crescentes para a origem polifilética da subfamília. As diferentes tribos e grupos de espécies que a compõem teri- am surgido recentemente, a partir de diferentes linhagens de reduviídeos. Palavras-chave Triatominae; Classificação; Evolução; Insetos Vetores Cad. Saúde Pública, Rio de Janeiro, 16(Sup. 2):89-92, 2000 90 SCHOFIELD, C. J. Introduction ferences of the host integument. Salivary func- tion must also be modified. The requirement The subfamily Triatominae (Hemiptera: Redu- of predators is for a toxic saliva that can rapid- viidae) is customarily organized into 5 tribes ly immobilize the invertebrate prey, whereas with 14 genera (Lent & Wygodzinsky, 1979; blood-suckers need a more benign saliva that Schofield, 1994), although three additional gen- will not stimulate adverse reactions from the era have recently been proposed (Carcavallo et vertebrate host (Schofield et al., 1986). Thus for al., 1998; Lent et al., 1994; Jurberg & Galvão, humans the bite of a predatory reduviid is gen- 1997). At present, 130 species are recognized erally very painful, and amongst the Triatomi- (Table 1), all characterized by an obligate blood- nae a painful bite – such as that of Triatoma sucking habit and various associated adapta- rubrofasciata, whose bite can provoke anaphy- tions including modifications of the mouth- lactic shock – can be considered a primitive parts, saliva, and digestive functions. The sub- character (cf. Ryckman & Bentley 1979; Ribeiro family is defined as a collection of hemato- et al., 1998). phagous Reduviidae (Jeannel, 1919), although At the level of digestion, a whole series of it is increasingly apparent that this assemblage physiological adaptations is required for an ob- is rather artificial and is probably unsustain- ligate hematophage (see Lehane, 1991). Blood able as a monophyletic grouping (Schofield, is a nutritionally rich resource, but it is highly 1988). For example, the two main tribes – Tria- alkaline, and much of the protein is locked in tomini and Rhodniini – seem to have little in the blood cells. Consequently the Triatominae common other than a basic reduviid form over- require both a hemolysin to open the blood laid with convergent characters associated with cells and a system to acidify the blood meal be- a blood-sucking diet. Apart from their differ- fore it can be digested. Reduviidae are derived ences in morphology (Lent & Wygodzinsky, from plant-sucking Hemiptera which have lost 1979) these two tribes show consistent differ- the ability to secrete trypsin, the usual diges- ences in sensorial patterns (Catalá, 1997; Cata- tive protease, because plant sap has virtually lá & Schofield, 1994), salivary gland physiology no protein, and plant seeds have potent anti- (Ribeiro et al., 1998), and DNA analysis (Garcia trypsins (Schofield, 1996). Thus the Reduviidae, et al., 1998; Stothard et al., 1998; Lyman et al., including Triatominae, must make use of se- 1999) and have probably originated from quite creted cathepsins as proteases, which are gen- different predatory forms. The Indian genus erally active only at acid pH. Blood is also gen- Linshcosteus seems to have evolved indepen- erally deficient in certain vitamins, particularly dently from the New World species of Triatomi- folate and B-vitamins, so that all obligate blood- nae (Gorla et al., 1997) and so probably merits suckers require symbionts to assist in produc- independent tribal status. ing these compounds. These symbionts are so Several lines of evidence support the idea important that all other obligate blood-suckers that the Triatominae have evolved relatively re- carefully conserve them either intracellularly cently from various of the predatory reduviids or in a special organ known as the mycetome. (Schofield, 1988; Schofield & Dolling, 1993). The But in Triatominae these symbionts are free in evolution of these blood-sucking forms can be the gut lumen, which is taken as additional evi- envisaged through a transitional phase of nest- dence that the blood-sucking habit is a relative- dwelling forms initially feeding on the guilds of ly recent adaptation (Schofield & Dolling, 1993). nest-dwelling invertebrates but progressively The process of speciation within the Tri- adapting to exploit the vertebrate nest-build- atominae is not well understood, but is subject ing host itself. Such a transition brings several to a major research effort because it encom- advantages, especially in terms of protection passes the processes by which Triatominae can from other predators and from climatic ex- adapt from sylvatic to domestic environments tremes, as well as the more reliable supply of – and so assume greater significance as vectors protein-rich food. The improved food supply of Chagas disease to humans. By morphologi- and protection from climatic extremes mean cal, biochemical, and genetic criteria, the dif- that reproduction becomes less dependent on ferent genera and species of Triatominae seem seasonal changes, and population density can to form a series of species groups, which gen- increase up to the limits of the available nutri- erally show a discrete geographical distribu- tion. However, the transition also requires sev- tion. This is additional evidence for their poly- eral adaptations. Mouthparts of predators are phyletic origins, which is now being supported generally robust and strongly chitinized (often by physiological comparisons and by genetic curved), whereas those of blood-sucking forms analysis based on isoenzymes and RAPD pro- are slim and slender, reflecting the physical dif- files (Garcia et al., 1998), as well as sequence Cad. Saúde Pública, Rio de Janeiro, 16(Sup. 2):89-92, 2000 BIOSYSTEMATICS AND EVOLUTION 91 analysis of ribosomal and mitochondrial DNA Table 1 (Garcia & Powell, 1998; Stothard et al., 1998; Ly- man et al., 1999). We can assume that amongst Tribes and Genera of the Triatominae (Hemiptera: Reduviidae). sylvatic species of Triatominae, natural selec- tion may play an important role in speciation, Tribe Genus No. species so that many species and species groups have adapted to highly specific host and habitat as- Alberproseniini Alberprosenia 2 sociations. Well-known examples include Ca- Bolboderini Belminus 6 vernicola pilosa which is invariably found in Bolbodera 1 bat caves, and species of Psammolestes which Microtriatoma 2 are invariably associated with the woven-stick Parabelminus 2 nests of furnariid weaver birds. In contrast, Cavernicolini Cavernicola 2 there are many groups of sylvatic species that Torrealbaia 1 remain relative generalists, such as the Tria- toma sordida group which can be found in a Rhodniini Psammolestes 3 very wide range of habitats. To a certain extent, Rhodnius 14 species can be ranked in accordance with their Triatomini Dipetalogaster 1 degree of adaptation to more stable habitats, Eratyrus 2 such as the domestic environment, and it may Linshcosteus 5 be that the more generalist species represent Panstrongylus 13 those which still have the potential for further Paratriatoma 1 adaptation to more specific habitats. Triatoma 75* Studies of Triatoma infestans and Rhodnius Total 130 prolixus, the two most widespread domestic species, reveal a further adaptive process which * 1) Note that some authors place Triatoma spinolai in a separate genus, Mepraia, following Lent et al. (1994). However, acceptance of this taxon would seems of major importance. In the case of T. in- leave unresolved the position of Triatoma breyeri and Triatoma eratyrusiformis, festans, true sylvatic populations are known on- which have been classed within the spinolai group (Lent & Wygodzinsky, 1979; Schofield, 1988). Frias et al. (1998) have denoted northern Chilean populations ly from the Cochabamba/Sucre region of cen- of T. spinolai (approximately from 18oS to 26oS) as Mepraia gajardoi. tral Bolivia, where bugs can be found amongst 2) Jurberg & Galvão (1997) place Triatoma matsunoi in a separate genus, rock piles associated with wild guinea pigs. Hermanlentia. Elsewhere, this species is almost exclusively domestic, although peridomestic populations can also be found in regions with a climate sim- ilar to that of central Bolivia. Comparison of T. ica. The Central American populations are al- infestans populations from many different lo- so smaller than their South American cousins, calities reveals that each has a generally low and show a highly restricted genetic repertoire level of population variability (in fact, they as revealed by RAPD profiles (Dujardin et al., have been likened to pseudo-clones), but there 1998b). In this case, the differences seem to re- are detectable genetic and phenetic differences flect a series of genetic bottlenecks and subse- between panmictic populations.