Formal Assignation of the Kissing Bug Triatoma lecticularia (Hemiptera: Reduviidae: Triatominae) to the Genus Paratriatoma ^†

Simple Summary

The genus Paratriatoma is closely related to the paraphyletic genus Triatoma—the most diverse and relevant in the epidemiology of Chagas disease. Molecular phylogenetic treatments consistently place the species Triatoma lecticularia (Stål, 1859) as a sister to the genus Paratriatoma. To determine its correct taxonomic assignment, we examined the morphology of several specimens, including types, and cytogenetic data for both taxa. The observations clearly support the transfer of Triatoma lecticularia (Stål, 1859) to the genus Paratriatoma, with the resulting new combination: Paratriatoma lecticularia (Stål, 1859) comb. nov. (Hemiptera: Heteroptera: Reduviidae: Triatominae).

Abstract

The subfamily Triatominae (Hemiptera: Reduviidae) comprises hematophagous insects that are vectors of Chagas disease; including species assigned to the genera Triatoma and Paratriatoma. Initial examination of Triatoma lecticularia revealed the hirsuteness covering the entire body—a characteristic and striking feature of members of the genus Paratriatoma—and a systematic study revealed several other morphological characters that are in diagnostic alignment with Paratriatoma. Based on the examination of several specimens (including the lectotype), and with the additional support of molecular and cytogenetic data, we propose the formal transferal of Triatoma lecticularia (Stål, 1859) into the genus Paratriatoma with the resulting new combination: Paratriatoma lecticularia (Stål, 1859) comb. nov. (Hemiptera: Reduviidae: Triatominae).

1. Introduction

Hematophagous insects of the subfamily Triatominae can transmit Chagas disease (American Trypanosomiasis). Currently, the subfamily comprises five tribes, 18 genera and, 156 species [1,2]. The Tribe Triatomini Jeannel, 1919 includes the genera Dipetalogaster Usinger, 1939; Eratyrus Stål, 1859; Hermanlentia Jurberg and Galvão, 1997; Mepraia Mazza, Gajardo, and Jörg, 1940; Nesotriatoma Usinger, 1944; Panstrongylus Berg, 1879; Paratriatoma Barber, 1938; and Triatoma Laporte, 1832.

Of these, the paraphyletic genus Triatoma is the most diverse with 82 described species [1], and the most relevant in the epidemiology of Chagas disease [3]. Historically there have been disagreements concerning the subgeneric (formal and informal) rankings within Triatoma. Since the 1960s, species have been grouped into complexes and subcomplexes based on morphological, geographical, ecological, and, more recently by molecular data [4,5,6,7,8,9]. One of such groupings is the Triatoma lecticularia complex, which has been proposed to include the Neartic species—T. lecticularia (Stål, 1859), T. sanguisuga (LeConte, 1856), T. gerstaeckeri (Stål, 1859), T. indictiva Neiva, 1912, T. recurva (Stål, 1868), and T. rubida (Uhler, 1894) [4,8]. However, some studies show that the Triatoma lecticularia complex is not well supported [6,10].

Triatoma lecticularia was originally described as Conorhinus lecticularius, based on specimens from Carolina (Museum Schaumburg), India Orientalis (deposited in Musei Berolinensis) [11]. Triatoma lecticularia occulta (Neiva, 1911) and T. lecticularia floridana (Usinger, 1944) were subspecific morphotypes proposed by the authors for specimens that showed a small variation in some morphological characters, such as the size of the head and eyes and the color pattern of the body [12,13]. Typical T. lecticularia specimens have an elongate-oval, shiny body, with the entire surface clothed by distinct decumbent hairs. Overall color piceous, with orange or orange-yellow markings on pronotum, pleura, corium, connexivum, and ventral surface of the abdomen [11]. It presents karyotype 2n = 22 (20A + XY), the same as Paratriatoma [14].

The genus Paratriatoma is closely related to Triatoma and can be distinguished by the ovoid shape of the head, absence of arcuate interocellar sulcus, absence of femoral spines or tubercles, and, mainly, by the remarkable hirsuteness of the body and the appendages [15]. The monotypic species, Paratriatoma hirsuta Barber 1938 is closely associated with pack/wood rats of the genus Neotoma in the Sonora Desert [16]. Five subspecies (P. hirsuta hirsuta, P. h. kamiensis Ryckman 1967, P. h. papagoensis Ryckman 1967, P. h. pimae Ryckman 1967, and P. h. yumanensis Ryckman 1967) have been described based on noted differences in coloration of the wings and head [17]. Subsequent analysis revealed that each subspecies represents a chromatic form, and is restricted to a limited geographical area [4].

In the current study, we show that the morphology of Triatoma lecticularia reconciled with molecular and cytogenetic data are entirely concordant with the genus Paratriatoma Barber, 1938 [3,18,19], and propose the new combination: Paratriatoma lecticularia (Stål, 1859), comb. nov. (Hemiptera: Heteroptera: Reduviidae: Triatominae).

2. Material and Methods

2.1. Material Examined

The male lectotype of T. lecticularia deposited in the Humboldt Museum für Naturkunde, Berlin, Germany (Figure 1,

Table 1. Information about the specimens examined, including the collection that is deposited.

Scheme 2920	Collection	Additional Information
Paratriatoma lecticularia comb. nov.	Humboldt Museum für Naturkunde, Berlin, Germany.	Male, Lectotypus, 2920
Paratriatoma lecticularia comb. nov.	José Manuel Ayala-Landa personal collection	San Antonio, TX 78201, USA, Female
Paratriatoma lecticularia comb. nov.	Triatomine collection “José Maria Soares Barata”, Universidade Estadual Paulista (UNESP), Brazil.	Male and female, CTA137
Paratriatoma hirsuta	U.S. National Entomological Collection, National Museum of Natural History, Smithsonian Institution, Washington DC	Type No. 52747 USNM, UCR_ENT 00007957, Mojave Cal.8.23.35
Paratriatoma hirsuta	Coleção de Triatomíneos do Instituto Oswaldo Cruz, Fiocruz, Brazil.	Male, H. Lent det., CTIOC 11976, N° 2729. Female Coleção Rodolfo Carcavallo, n° 1724, CTIOC N° 6229
Paratriatoma hirsuta	Coleção Entomológica de Referência, Faculdade de Saúde Pública, Universidade de São Paulo, Brazil	Female Suporte 141, tubo 2 n° E5027 Desert Center, Calif. Riverside Couty 28/11/50. Col. R.E. Ryckman. Female Suporte 141, tubo 1 n° E5026 Desert Center, Calif. Riverside Couty 28/11/50. Col. R.E. Ryckman. Reared 1952
Paratriatoma hirsuta	José Manuel Ayala-Landa personal collection	Joshua Tree National Park, USA- California. Female.

), and five males and five females of T. lecticularia deposited in Triatomine collection “José Maria Soares Barata”, Universidade Estadual Paulista (UNESP), Araraquara, São Paulo, Brazil (Figure 2, Figure 3 and Figure 4, Table 1), were directly examined. The type specimen of Paratriatoma hirsuta deposited in U.S. National Entomological Collection, National Museum of Natural History, Smithsonian Institution, Washington DC, was also studied. Four specimens of P. hirsuta deposited in the “Coleção de Triatomíneos do Instituto Oswaldo Cruz, Fiocruz, Brazil” (Figure 5, Table 1), two specimens of “Coleção Entomológica de Referência, Faculdade de Saúde Pública, Universidade de São Paulo, Brazil” (Figure 6, Table 1), and ten specimens deposited in Ayala-Landa personal collection (Figure 7, Table 1), were used to compare with T. lecticularia.

2.2. Morphological Study

Photographs were made using a professional camera and Leica M205C stereomicroscope and were processed with the software Leica LAS (version 4.9). Type specimens were examined through photographs, and label information is provided (Table 1). Based on Barber’s original (1938) description of the genus Paratriatoma, the major features distinguishing Paratriatoma from species in Triatoma include the ovoidal shape of the head, the absence of an arcuate interocellar sulcus, the absence of femoral spines or tubercles, and the intensely hirsute body and appendages. Another apomorphy is noted in the plates of the dorsal and ventral connexivum of the urosternite overlapping the mesal portion of the ventral plate of the connexivum, with a distinct membrane interpolated between the edge of the connexival plate and the lateral edge of the urosternum (Figure 8).

3. Results

3.1. Taxonomic Hierarchy

Class Insecta Linnaeus, 1758, Order Hemiptera Linnaeus, 1758, Family Reduviidae Latreille, 1807, Subfamily Triatominae Jeannel, 1919, Tribe Triatomini Jeannel, 1919, Genus Paratriatoma lecticularia (Stål, 1859), comb. nov. (Figure 1).

Synonyms

Conorhinus lecticularius Stål, 1859 [original description]; Conorhinus lenticularius Stål, 1868; Conorhinus variegatus Stål, 1872; Conorhinus heidemanni Patton and Cragg, 1913; Conorhinus occulata Patton and Cragg, 1913; Conorhinus lectularius Neiva, 1914; Triatoma heidemanni Neiva, 1911, 1914. Blatchley, 1926. Pinto, 1931. Usinger, 1943; Triatoma occulta Neiva, 1911, 1914; Triatoma sanguisuga Neiva, 1914; Triatoma lecticularius Usinger, 1944; Triatoma lecticularius occulta Usinger, 1944; Triatoma lecticularius floridana Usinger, 1944.

3.2. Morphological Characterization of Paratriatoma

Ovoidal shape of the head, scarcely shorter than the pronotum. Eyes rather, small not strongly projected. Anteocular region longer than postocular, transversely impressed behind the strongly elevated clypeus. Ocelli slightly elevated, widely separated. Antennae inserted closer to the eyes than to the apex of the head, as in Triatoma. Pronotum somewhat wider than long. Scutellum devoid of a discal depressed area, prolonged into a cylindrical, apical process. Legs rather short, scarcely incrassate, mutic. The entire body and the appendages sparsely covered with long, coarse hairs.

3.3. Morphological Characterization of P. lecticularia comb. nov.

Coloration. Overall color piceous, with orange or orange-yellow markings on pronotum, pleura, corium, connexivum, and ventral surface of the abdomen (Figure 1, Figure 2, Figure 3 and Figure 4). Head uniformly dark, neck uniformly light in color (Figure 8). Pronotum dark with 1 + 1 orange bands on lateral margins of the posterior lobe, posterior margin of pronotum is lighter colored in some specimens; in some specimens, dark areas of the posterior lobe of pronotum reduced to one wide median and 1 + 1 sublateral stripes, with orange color extending as 1 + 1 wide lateral and 1 + 1 submedian spots occupying carinae and triangularly widened posteriorly, confluent behind with lateral markings (Figure 3 and Figure 4). Pleura dark. Scutellum dark. Corium with a large central spot of general color, with basal and subapical spots orange-yellow, and the outer border is narrowly bordered with light color. Legs dark, but with coxae in many cases lightened. Venter with orange-yellow markings at the level of light-colored connexival markings, covering intersegmental sutures and extending along lateral borders of urosternites; in some cases, the entire venter tinged with orange, especially on basal half (Figure 1, Figure 3, and Figure 4). Connexival segments dark, posteriorly with orange-yellow spot narrowly extending across intersegmental suture onto the anterior portion of the following segment; extension of light markings variable (Figure 1 and Figure 8B).

Morphological features. The body surface clothed with distinct decumbent hairs. Head (Figure 2 and Figure 8) granulose, ovoidal shape, conspicuously convex; slightly less than twice as long as width across eyes and slightly shorter than pronotum. Anteocular region about three times as long as postocular, postocular with sides convex, converging posteriorly. Eyes in lateral view attaining or slightly surpassing the level of under but not attaining the level of the upper surface of the head. Antenniferous tubercles situated on the posterior third of the anteocular region, comparatively close to the eyes. First antennal segment falling short of apex of clypeus. Rostrum conspicuously hairy, especially on second and third segments; first segment attaining a level of apex of antenniferous tubercle, second attaining level of the neck. The third segment of the rostrum smaller than the first, which is smaller than the second. Pronotum (Figure 1), narrow anteriorly, becoming wider posteriorly and extending onto humeri; posterior margin of pronotum possess submedian carinae and collar with anterolateral processes; Anterior lobe without discal or lateral tubercles. Posterior lobe rugose, with conspicuous dark setae on the entire surface; submedian carinae evanescent posteriorly. Humeral angles rounded, slightly elevated. Anterolateral angles short, rounded apically. Scutellum (Figure 1) with central portion only very slightly depressed, limited by irregular carinae; apical process shorter than the main body of scutellum, setose, tapering distally, its apex deflected. Hemelytra reaching nearly to the apex of the abdomen. Corium completely with conspicuous adpressed black setae. Legs hairy, rather short. Fore- and mid-femora with 2 + 2 very short denticles subapically. Tibiae of first and second pair in males with small spongy fossulae, absent in the female. Spiracles remote from connexival suture (Figure 9). Venter conspicuously pilose (Figure 1). Connexivum with distinct adpressed setae. In unfed specimens, the plates of the dorsal and ventral connexivum of the urosternite overlap the mesal portion of the ventral plate of the connexivum, with a distinct membrane interpolated between the edge of the connexival plate and the lateral edge of the urosternum (Figure 8). This membrane is not normally visible in museum specimens, in which the ventral plates of the connective appear exceptionally narrow, as they are partially covered by urosternites. Urosternites VIII, IX, and X form the female external genitalia (Figure 9).

A synonymized T. l. floridana form is distinguished by its paler coloration and large eyes. A synonymized T. l. occulta is an extreme form, smaller in body and eye size.

Vestiture. Pilosity is well developed on the entire body including the corium (Figure 1 and Figure 2).

4. Discussion

4.1. Transfer of Triatoma lecticularia to Paratriatoma

Stål (1859) described this species as Conorhinus lecticularius, and the specimen label states the locality as “India Orientalis” (Figure 1). The insect bears an obviously erroneous locality label because it does not inhabit the East Indies [4]. The type specimen was housed in the Berlin Museum. In 1872, Stål synonymized his lecticularius with variegatus, a synonym of rubrofasciata. Later, Neiva set lecticularius in the synonymy of sanguisuga [20]. Lent and Wygodzisnky synonymized the subspecies T. l. occulta and T. l. floridana with T. lecticularia, and later appointed a lectotype (Figure 1) [4].

The distribution of Paratriatoma lecticularia (Stål, 1859) comb. nov. includes the United States (Arizona, California, Florida, Georgia, Illinois, Kansas, Louisiana, Maryland, Missouri, New Mexico, South Carolina, Tennessee, and Texas) and Mexico (Nuevo Leon), in ecotopes with widely variable climatic conditions, from humid forests to valleys and deserts. The species is found associated with the terrestrial rodent Neotoma micropus Baird, and rock squirrel Spermophilus variagatus (Erxleben) [21], whereas Paratriatoma hirsuta (Figure 6 and Figure 7) is thought to be obligate ectoparasites of the pack rats or wood rats Neotoma lepida Thomas, Neotoma fuscipes macrotis Thomas, and Neotoma albigula Hartley. In human dwellings, Paratriatoma hirsuta is found under cracks in the wall, beds, and wooden hollows, and has been found naturally infected by Trypanosoma cruzi (Chagas, 1909) [16,21].

Lent and Wygodzinsky determined that the Triatoma lecticularia complex included T. lecticularia, T. sanguisuga, and T. indictiva [4] and later Schofield and Galvão [8] added T. gerstaeckeri, T. recurva, and T. rubida to the complex. Monteiro et al. [6] proposed that the North American Clade (North of Tehuantepec) of Triatoma protracta (Uhler, 1894), Triatoma barberi Usinger, 1939, T. lecticularia, Paratriatoma hirsuta Barber, 1938, and Dipetalogaster maxima (Uhler, 1894) comprised a separate species group changing the classification of “complexes” of several species. Nevertheless, as hypothesized by Lent and Wygodzinsky [4], Paratriatoma is close to the Triatoma protracta complex, so the T. protracta complex can be considered one of the sister groups to Paratriatoma, despite having the membrane structure of the connexivum apomorphic (Figure 8).

Cytogenetically, the typical autosome number (A) in triatomines is 20. Paratriatoma lecticularia differs from other North American species in both chromosome complement and behavior of the sex chromosomes. Paratriatoma lecticularia presents the karyotype 2n = 22 (20A + XY)—the same as Paratriatoma hirsuta. All the other species in the T. lecticularia complex exhibit karyotype 2n = 23 (20A + X1 × 2Y). Considering that T. rubida present 2n = 23 and P. lecticularia and P. hirsuta 2n = 22, it was hypothesized that the ancestor of these triatomines had 22 chromosomes, and during the divergence of T. rubida and others, probably an agmatoploidy of the X sex chromosome occurred [14,19].

Justi et al. [3] performed a molecular phylogeny of Triatomini, recovering a clade that includes the genera Hermanlentia, Paratriatoma, and Dipetalogaster + Linshcosteus + Northern Hemisphere Triatoma (BS = 88, PP = 1); P. hirsuta + P. lecticularia were considered sister species in the phylogeny. Using Bayesian analysis (with six fossils calibrations), Justi et al. [18] proposed P. hirsuta and P. lecticularia as sister species (with high support = 1). Kieran et al. [22] analyzed 40 species of Triatomini using Ultraconserved Elements (UCEs) and ribosomal dataset, and based on the best likelihood tree concluded that Paratriatoma hirsuta and P. lecticularia are sister species and are included in the protracta clade.

In addition to the morphological characters mentioned in the results, reconstruction of the ancestral character state of the fossula spongiosa in males puts P. hirsuta and P. lecticularia in the same clade [22] and, the structure of the plates and membrane of connexivum are characteristic of Paratriatoma (Figure 8), being apomorphic with the Triatomini tribe. Combining morphological, molecular, and cytogenetic data, it is clear that Paratriatoma lecticularia comb. nov. does not belong to Triatoma.

Paratriatoma lecticularia occurs from the south-central to the Atlantic coast of the USA and can be collected in houses, kennels, woodrat nests (Neotoma), and squirrels. It has been reported as a nuisance species, commonly found in well-built dwellings in central Texas. Paratriatoma hirsuta occurs in the western United States, collected from arid regions in woodrat nests and human dwellings, and has been described as “attacking human”, in addition to being of public health importance due to allergic reactions caused by its bite [13,23]. Both species proved to be a competent vector of T. cruzi experimentally. Colonization and invasion of dwellings by triatomines is an important factor in vector transmission, as it increases the chance of feeding potentially infected vectors in humans [23,24]. With the marked loss of their habitats, caused by deforestation and unplanned urbanization, major changes in the epidemiology of Chagas disease are expected. However, we know that a strong and sustained surveillance system is the best strategy. In this dynamic world, making predictions is not easy, so with all the knowledge about the biology, morphological, molecular, and cytogenetic taxonomy of triatomine, we can plan public health control in a world with an uncertain future [25].

4.2. Dichotomous Key for Species of Paratriatoma

Head, body, and appendages with numerous broad, curved, semi-erect setae; head very strongly convex dorsally; small eyes; antenniferous tubercles inserted near the anterior edge of the eye; anterior femurs without denticles; absent spongy fossulae; legs short and robust, the posterior femurs less than six times longer than broad; first segment of the rostrum less than twice the length of the third; general body coloration light to dark brown Paratriatoma hirsuta (Figure 5, Figure 6 and Figure 7).

Head strongly convex dorsally, especially between eyes; antenniferous tubercles elongate, comparatively close to eyes; body clothed with numerous black setae, conspicuous on head; overall color piceous, with orange or orange-yellow markings on pronotum, pleura, corium, connexivum, and ventral surface of abdomen; tibiae of first and second pair in males with small spongy fossulae, absent in female Paratriatoma lecticularia (Figure 1, Figure 2, Figure 3 and Figure 4).

5. Conclusions

The genus Paratriatoma is closely related to the paraphyletic genus Triatoma—the most diverse and relevant in the epidemiology of Chagas disease. Initial examination of Triatoma lecticularia revealed the hirsuteness covering the entire body—a characteristic and striking feature of members of the genus Paratriatoma—and a systematic study revealed several other morphological characters that are in diagnostic alignment with Paratriatoma. Molecular phylogeny treatments consistently place the species Triatoma lecticularia (Stål, 1859) as sister to the genus Paratriatoma. To determine its correct taxonomic assignment, we examined the morphology of several specimens, including types, and cytogenetic data for both taxa. The observations clearly support the formal transferal of Triatoma lecticularia (Stål, 1859) into the genus Paratriatoma with the resulting new combination: Paratriatoma lecticularia (Stål, 1859) comb. nov. (Hemiptera: Reduviidae: Triatominae).