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Heteroptera: Reduviidae) Fernando Otálora-Luna1*, Antonio J Pérez-Sánchez1, Claudia Sandoval1 and Elis Aldana2

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Heteroptera: Reduviidae) Fernando Otálora-Luna1*, Antonio J Pérez-Sánchez1, Claudia Sandoval1 and Elis Aldana2 Otálora-Luna et al. Revista Chilena de Historia Natural (2015) 88:4 DOI 10.1186/s40693-014-0032-0 REVIEW Open Access Evolution of hematophagous habit in Triatominae (Heteroptera: Reduviidae) Fernando Otálora-Luna1*, Antonio J Pérez-Sánchez1, Claudia Sandoval1 and Elis Aldana2 Abstract All members of Triatominae subfamily (Heteroptera: Reduviidae), potential vectors of Trypanosoma cruzi, etiologic agent of the Chagas disease, feed on blood. Through evolution, these bugs have fixed special morphological, physiological, and behavioral aptations (adaptations and exaptations) adequate to feed on blood. Phylogeny suggests that triatomines evolved from predator reduvids which in turn descended from phytophagous hemipterans. Some pleisiomorphic traits developed by the reduvid ancestors of the triatomines facilitated and modeled hematophagy in these insects. Among them, mouthparts, saliva composition, enzymes, and digestive symbionts are the most noticeable. However, the decisive step that allowed the shift from predation to hematophagy was a change of behavior. The association of a predator reduvid with nesting vertebrate (≈110 to 32 Ma) permitted the shift from an arthropod prey to a vertebrate host. In this work, we review the phylogeny and dispersion of triatomines and the current controversy over the monophyly or polyphyly of this group. We also discuss how these insects were able to overcome, and even have taken advantage of, diverse ancestral and physical barriers to adapt to sucking blood of nidicolous vertebrates. We provide a Spanish version of this work. Keywords: Latin America; Chagas' disease; Phylogeny; Blood-sucking habit; Triatomines Introduction due to their clear involvement in the domestic and peri- The triatomines are an insect subfamily of the Reduviidae domestic transmission cycles. The species Triatoma infes- family in the Hemiptera order, known by various names tans (Klug), Rhodnius prolixus (Stål), Triatoma dimidiata in different regions of America, among which the most (Latreille), and Triatoma brasiliensis (Neiva) are recog- common are as follows: vinchuca (from Ecuador to nized as the principal vectors in Latin America (Lent and Patagonia), chipo (Venezuela), pito (Colombia), barbeiro Wygodzinsky 1979; Bargues et al. 2010; Rabinovich et al. (Brazil), chinche (Central America and Mexico), and kis- 2011; Stevens et al. 2011). sing bug (USA) (Lent and Wygodzinsky 1979; Schofield The hematophagic habit has marked the natural his- and Galvão 2009). The members of this subfamily are tory of the triatomines. Furthermore, this habit has almost entirely hematophagous, although there are stamped them with striking anthropological importance, cases of some species that feed on other invertebrates given that this was what included them in the parasite's (Sandoval et al. 2004, 2010). It is known that triatomines life cycle and eventually humans as well, as hosts. How live together with nidicolous (nesting) vertebrates, whose the triatomines got to be bloodsuckers depended on the blood they extract for nourishment, and certain species genetic complex these organisms inherited from their infest human homes and buildings (Noireau and Dujardin non-hematophagous ancestors by means of different 2010). All triatomines species are considered potential evolutionary mechanisms that have been suggested, and vectors of the Trypanosoma cruzi (Chagas) parasite, the the restrictions imposed by their physical surroundings etiological agent of the Chagas' disease; nonetheless, only (sensu Dusenbery 2001; Figure 1). In addition to consid- about 20 species are considered of epidemical importance ering the adaptive value of certain morphological, physiological, and behavioral traits associated with this * Correspondence: [email protected] habit, it is necessary to take into consideration how the 1Laboratorio de Ecología Sensorial, Centro Multidisciplinario de Ciencias, Instituto Venezolano de Investigaciones Científicas, (IVIC), Loma de Los physical and chemical laws that have governed the uni- Guamos, Mérida, República Bolivariana de Venezuela verse's functioning made possible its appearance. In Full list of author information is available at the end of the article © 2015 Otálora-Luna et al.; licensee Springer. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. Otálora-Luna et al. Revista Chilena de Historia Natural (2015) 88:4 Page 2 of 13 Figure 1 Historical and physical-chemical interaction between the environment and triatomines. Due to the historical and physical- chemical interaction that occurred between the environment and triatomines, several adaptations and exaptations have appeared and changed, and such changes have been fixed as genetic information. These interactions are illustrated by the three arrows on the left. It is difficult to illustrate how natural history is the product (in part) of the interactions that have occurred, in evolutionary time, between the triatomines and the environment. In any case, the arrow on the right illustrates how at least part of the natural history, which may include the geological and climatic history (including the physical-chemical factors), has been registered in the triatomines genome. other words, given that the phenotypical expression is not find refuge, and in some cases, food; (ii) ability to fly in limited only by restrictions on their functioning but also by the adult stage (for the majority of the species), an import- the way they were made (physical restraints) and by their ant characteristic for the explotation of new and better re- past (historical and phylogenetic limits), it must be sup- sources; (iii) a highly concentrated nervous system which posed that the driven force could be as much historical- permits fast and varied movements; and (iv) the presence genetic as environmental (sensu De Renzi 2009; Dusenbery 2001; Figure 1). The theory of functional morphology or Table 1 Time of emergence of hemipteroid insects and biomorphodynamics has advanced considerably towards some warm blooded vertebrates this neo-evolutionary line of thinking (De Renzi 2009) and Era Period Epoch Date Originated group (Ma) has allowed us to understand better the triatomines' (Ma) evolution (e.g., González et al. 2009). This review will offer Cenozoic Quaternary Holocene 0.012 Triatomines domiciliation a sketch of the phylogeny and radiation of the group and Pleistocene 2.6 will show how these insects could have overcome, and even taken advantage of, several physical and ancestral Neogene Pliocene 5.3 barriers to adapt to bloodsucking of a nidicolous host. We Miocene 23 (Nidicolous vertebrates discuss how the step from preying to bloodsucking was diversification) influenced by, among other things, a change of behavior of Paleogene Oligocene 34 the reduvidian ancestors of the triatomines. We provide a Eocene 55 Spanish version of this work (Additional file 1). Paleocene 65 Triatominae (≈32 to 110)a Review Mesozoic Cretaceous 144 Birds (≈150) Triatomines phylogeny Jurassic 206 Mammals (≈200) Hemiptera Triassic 250 The beginnings of the Hemiptera order go back to the Reduviidae (≈230) late Carboniferous, 300 million years ago (Ma), with fos- sils dated to the Early Permian (Wootton 1981; Burmester Paleozoic Permian 290 Hemiptera (≈300) 2001; Grimaldi and Engel 2005; Table 1). Nearly 82,000 Carboniferous 354 species have been described within this monophyletic Devonian 417 order, and it is by far the largest group of hemimetabolic Silurian 443 insects, whose diversity is probably related to the radiation Ordovician 490 of the angiosperms (Gillot 2005; Grimaldi and Engel 2005; Cambrian 543 Forero 2008). According to Dolling (1991), the success of The geological data correspond to millions of years (Ma). aThere is a broad debate hemipterans could be based on the following characteris- about the date of origin of Triatominae; for more information, see the text. tics: (i) compact flat bodies, a trait which allows them to Otálora-Luna et al. Revista Chilena de Historia Natural (2015) 88:4 Page 3 of 13 of a piercing-sucking buccal mechanism by means of Predation is common in heteropters, and many of the which they can access various vegetal fluids and animal families consist totally of insect predators (entomophages) tissues. In this sense, it is believed that the first Hemiptera that occupy a broader range of habitats than the other were phytophagous and both that entomophagy and phytophagic members. The hematophagy appears to have hematophagy evolved from these sap and phloem-sucking risen more than once stemming from predator hete- insects (Grimaldi and Engel 2005). ropters. Some families, like Cimicidae, Polyctenidae, and Reduviidae, have developed the capacity to feed on vertebrate blood (Lehane 2005). Cimicidae (bedbugs) Heteroptera feed exclusively on vertebrate blood, usually of birds, bats, Traditionally, the Hemiptera order has been divided in and human beings; while all the members of the small two groups or suborders, Homoptera (Sternorrhyncha Polyctenidae family (e.g. Eoctenes spasmos Waterhouse) and Auchenorrhyncha) and Heteroptera, which includes feed on bats in both the Old and the New World (Kim the triatomines (Dolling 1991; Gillot 2005). With nearly 1985; Lehane 2005). Within the Reduviidae, the members 40,000 known species, Heteroptera is sometimes accep- of
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