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. 2021 Dec 15;10(12):1627. doi: 10.3390/pathogens10121627

Trends in Taxonomy of Chagas Disease Vectors (Hemiptera, Reduviidae, Triatominae): From Linnaean to Integrative Taxonomy

Kaio Cesar Chaboli Alevi 1,2,3, Jader de Oliveira 1,2, Dayse da Silva Rocha 3, Cleber Galvão 3,*
Editors: Lawrence S Young, Rubén Bueno-Marí, Daniel Bravo-Barriga, Rodrigo Morchón
PMCID: PMC8706908  PMID: 34959582

Abstract

Chagas disease is a neglected tropical disease caused by the protozoan Trypanosoma cruzi and transmitted mainly by members of the subfamily Triatominae. There are currently 157 species, grouped into 18 genera and five tribes. Most descriptions of triatomine species are based on classical taxonomy. Facing evolutionary (cryptic speciation and phenotypic plasticity) and taxonomic (more than 190 synonymizations) problems, it is evident that integrative taxonomy studies are an important and necessary trend for this group of vectors. Almost two-and-a-half centuries after the description of the first species, we present for the first time the state-of-the-art taxonomy of the whole subfamily, covering from the initial classic studies to the use of integrative taxonomy.

Keywords: Triatominae, classical taxonomy, molecular taxonomy, integrative taxonomy

1. Triatominae: The Vectors of Chagas Disease

Chagas disease is a neglected tropical disease caused by the protozoan Trypanosoma cruzi (Chagas, 1909) (Kinetoplastida, Trypanosomatidae) [1]. This disease is found mainly in 21 Latin American countries, where it is mostly vector-borne, more specifically by members of the subfamily Triatominae (Hemiptera, Reduviidae) [1]. Triatomines or kissing bugs are hematophagous insects that have a habit of defecating during or after the blood meal—if they are infected with T. cruzi, they release the parasite in the feces/urine [1]. An estimated 8 million people are infected worldwide, and more than 65 million people at risk of acquiring the disease, which causes more than 12,000 deaths per year, the vector control being the most useful method to prevent new infections [1,2].

There are currently 157 species (154 extant species and three fossils), grouped into 18 genera and five tribes (Table 1) [3,4,5,6,7], being all potential vectors of T. cruzi. Taxonomic studies of Triatominae started in the 18th century with the description of Triatoma rubrofasciata (De Geer, 1773) (as Cimex rubro-fasciatus) [8]. Almost two and a half centuries after the description of the first species, we presented for—the first time—a review of the state-of-the-art of taxonomy of the whole subfamily, covering from the initial classic studies to the use of integrative taxonomy, a term formally introduced only in 2005 to describe taxa by integrating information from different data and methodologies [9,10].

Table 1.

Tribes, genera, and number of species that make up the subfamily Triatominae.

Tribe Genus Species (n)
Alberproseniini Alberprosenia 2
Bolboderini Belminus 9
Bolbodera 1
Microtriatoma 2
Parabelminus 2
Cavernicolini Cavernicola 2
Rhodniini Psammolestes 3
Rhodnius 21
Triatomini Dipetalogaster 1
Eratyrus 2
Hermanlentia 1
Linshcosteus 6
Mepraia 3
Nesotriatoma 3
Panstrongylus 15
Paratriatoma 2
Triatoma 81
Paleotriatoma 1
Total 157
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2. Applications and Limitations of Triatominae Taxonomic Studies

For 225 years (1773–1998), the descriptions of triatomine species have been based only on studies of classical taxonomy (using descriptive morphology, comparative morphology, and/or morphometry) (Table 2). Although these analyses are imperative and are present in the description of all species of the subfamily Triatominae (Table 2), in the last decade, other approaches (such as biochemical [5,11], cytogenetic [5,12], phylogenetic [5,13,14,15,16,17] and/or of reproductive barriers [5]) started to be combined with the characterization of morphology and/or morphometry, employing the integrative taxonomy in the study of these insect vectors (Table 2).

Table 2.

Species, taxonomic tools, and taxonomic classification used in the description of Triatominae taxa.

Species Morphology and Morphometry Chemotaxonomy Cytotaxonomy Experimental Crosses Phylogenetic Systematics and Molecular Taxonomy Taxonomy References
1 Triatoma rubrofasciata (De Geer, 1773) X Classical taxonomy De Geer [8]
2 Triatoma dimidiata (Latreille, 1811) X Classical taxonomy Latreille [21]
3 Panstrongylus geniculatus (Latreille, 1811) X Classical taxonomy Latreille [21]
4 Triatoma infestans (Klug, 1834) X Classical taxonomy Klug [22]
5 Triatoma phyllosomus (Burmeister, 1835) X Classical taxonomy Burmeister [23]
6 Panstrongylus megistus (Burmeister, 1835) X Classical taxonomy Burmeister [23]
7 Triatoma rubrovaria (Blanchard, 1846) X Classical taxonomy Blanchard [24]
8 Triatoma maculata (Erichson, 1848) X Classical taxonomy Erichson [25]
9 Triatoma mexicana (Herrich-Schaeffer, 1848) X Classical taxonomy Herrich-Schaeffer [26]
10 Triatoma sanguisuga (Leconte, 1855) X Classical taxonomy Leconte [27]
11 Belminus rugulosus (Stål, 1859) X Classical taxonomy Stål [28]
12 Eratyruscuspidatus (Stål, 1859) X Classical taxonomy Stål [28]
13 Eratyrusmucronatus (Stål, 1859) X Classical taxonomy Stål [28]
14 Rhodnius nasutus (Stål, 1859) X Classical taxonomy Stål [28]
15 Rhodnius prolixus (Stål, 1859) X Classical taxonomy Stål [28]
16 Triatoma circummaculata (Stål, 1859) X Classical taxonomy Stål [28]
17 Triatoma gerstaeckeri (Stål, 1859) X Classical taxonomy Stål [28]
18 Paratriatoma lecticularia (Stål, 1859) X Classical taxonomy Stål [28]
19 Triatoma sordida (Stål, 1859) X Classical taxonomy Stål [28]
20 Triatoma vitticeps (Stål, 1859) X Classical taxonomy Stål [28]
21 Triatoma recurva (Stål, 1868) X Classical taxonomy Stål [29]
22 Triatoma venosa (Stål, 1872) X Classical taxonomy Stål [30]
23 Triatoma pallidipennis (Stål, 1872) X Classical taxonomy Stål [30]
24 Rhodnius pictipes (Stål, 1872) X Classical taxonomy Stål [30]
25 Triatoma nigromaculata (Stål, 1872) X Classical taxonomy Stål [30]
26 Panstrongylus lignarius (Walker, 1873) X Classical taxonomy Walker [31]
27 Panstrongylus guentheri (Berg, 1879) X Classical taxonomy Berg [32]
28 Triatoma rubida (Uhler, 1894) X Classical taxonomy Uhler [33]
29 Dipetalogaster maxima (Uhler, 1894) X Classical taxonomy Uhler [33]
30 Triatoma protracta (Uhler, 1894) X Classical taxonomy Uhler [33]
31 Panstrongylus rufotuberculatus (Champion, 1899) X Classical taxonomy Champion [34]
32 Triatoma migrans (Breddin, 1903) X Classical taxonomy Breddin [35]
33 Linshcosteuscarnifex (Distant, 1904) X Classical taxonomy Distant [36]
34 Bolbodera scabrosa (Valdés, 1910) X Classical taxonomy Valdés [37]
35 Nesotriatoma flavida (Neiva, 1911) X Classical taxonomy Neiva [38]
36 Psammolestes coreodes (Bergroth, 1911) X Classical taxonomy Bergroth [39]
37 Panstrongylus howardi (Neiva, 1911) X Classical taxonomy Neiva [40]
38 Triatoma brasiliensis (Neiva, 1911) X Classical taxonomy Neiva [41]
39 Triatoma neotomae (Neiva, 1911) X Classical taxonomy Neiva [42]
40 Triatoma indictiva (Neiva, 1912) X Classical taxonomy Neiva [43]
41 Triatoma platensis (Neiva, 1913) X Classical taxonomy Neiva [44]
42 Rhodnius brethesi (Matta, 1919) X Classical taxonomy Matta [45]
43 Panstrongylus lutzi (Neiva & Pinto, 1923) X Classical taxonomy Neiva and Pinto [46]
44 Rhodnius domesticus (Neiva & Pinto, 1923) X Classical taxonomy Neiva and Pinto [47]
45 Triatoma melanocephala (Neiva & Pinto, 1923) X Classical taxonomy Neiva and Pinto [48]
46 Triatoma bouvieri (Larrousse, 1924) X Classical taxonomy Larrousse [49]
47 Triatoma petrocchiae (Pinto & Barreto, 1925) X Classical taxonomy Pinto and Barreto [50]
48 Psammolestes arthuri (Pinto, 1926) X Classical taxonomy Pinto [51]
49 Triatoma carrioni (Larrousse, 1926) X Classical taxonomy Larrousse [52]
50 Triatoma tibiamaculata (Pinto, 1926) X Classical taxonomy Pinto [53]
51 Rhodnius robustus (Larrousse, 1927) X Classical taxonomy Larrousse [54]
52 Panstrongylus chinai (Del Ponte, 1929) X Classical taxonomy Del Ponte [55]
53 Triatoma breyeri (Del Ponte, 1929) X Classical taxonomy Del Ponte [55]
54 Triatoma eratyrusiformis (Del Ponte, 1929) X Classical taxonomy Del Ponte [55]
55 Triatoma limai (Del Ponte, 1929) X Classical taxonomy Del Ponte [55]
56 Triatoma patagonica (Del Ponte, 1929) X Classical taxonomy Del Ponte [55]
57 Rhodnius pallescens (Barber, 1932) X Classical taxonomy Barber [56]
58 Triatoma leopoldi (Schoudeten, 1933) X Classical taxonomy Schoudeten [57]
59 Mepraia spinolai (Porter, 1934) X Classical taxonomy Porter [58]
60 Cavernicola pilosa (Barber, 1937) X Classical taxonomy Barber [59]
61 Paratriatoma hirsuta (Barber, 1938) X Classical taxonomy Barber [60]
62 Triatoma longipennis (Usinger, 1939) X Classical taxonomy Usinger [61]
63 Triatoma picturatus (Usinger, 1939) X Classical taxonomy Usinger [61]
64 Panstrongylus humeralis (Usinger, 1939) X Classical taxonomy Usinger [61]
65 Triatoma barberi (Usinger, 1939) X Classical taxonomy Usinger [61]
66 Triatoma incrassata (Usinger, 1939) X Classical taxonomy Usinger [61]
67 Triatoma nitida (Usinger, 1939) X Classical taxonomy Usinger [61]
68 Triatoma oliveirai (Neiva et al., 1939) X Classical taxonomy Neiva et al. [62]
69 Triatoma arthurneivai (Lent & Martins, 1940) X Classical taxonomy Lent and Martins [63]
70 Triatoma hegneri (Mazzotti, 1940) X Classical taxonomy Mazzotti [64]
71 Triatoma peninsularis (Usinger, 1940) X Classical taxonomy Usinger [65]
72 Triatoma mazzottii (Usinger, 1941) X Classical taxonomy Usinger [66]
73 Triatoma melanica (Neiva & Lent, 1941) X Classical taxonomy Neiva and Lent [67]
74 Panstrongylus tupynambai (Lent, 1942) X Classical taxonomy Lent [68]
75 Parabelminus carioca (Lent, 1943) X Classical taxonomy Lent [69]
76 Panstrongylus diasi (Pinto & Lent, 1946) X Classical taxonomy Pinto and Lent [70]
77 Triatoma delpontei (Romaña & Abalos, 1947) X Classical taxonomy Romaña and Abalos [71]
78 Triatoma guasayana (Wygodzinsky & Abalos, 1949) X Classical taxonomy Wygodzinsky and Abalos [72]
79 Triatoma dispar (Lent, 1950) X Classical taxonomy Lent [73]
80 Triatoma wygodzinskyi (Lent, 1951a) X Classical taxonomy Lent [74]
81 Microtriatoma trinidadensis (Lent, 1951b) X Classical taxonomy Lent [75]
82 Triatoma amicitiae (Lent, 1951c) X Classical taxonomy Lent [76]
83 Rhodnius neivai (Lent, 1953) X Classical taxonomy Lent [77]
84 Triatoma matogrossensis (Leite & Barbosa, 1953) X Classical taxonomy Leite and Barbosa [78]
85 Triatoma pugasi (Lent, 1953b) X Classical taxonomy Lent [79]
86 Rhodnius neglectus (Lent, 1954) X Classical taxonomy Lent [80]
87 Belminus costaricencis (Herrer et al., 1954) X Classical taxonomy Herrer et al. [81]
88 Belminus peruvianus (Herrer et al., 1954) X Classical taxonomy Herrer et al. [81]
89 Rhodnius ecuadoriensis (Lent & León, 1958) X Classical taxonomy Lent and León [82]
90 Triatoma costalimai (Verano & Galvão, 1958) X Classical taxonomy Verano and Galvão [83]
91 Nesotriatoma obscura (Maldonado & Farr, 1962) X Classical taxonomy Maldonado and Farr [84]
92 Triatoma sinaloensis (Ryckman, 1962) X Classical taxonomy Ryckman [85]
93 Triatoma pseudomaculata (Corrêa & Espínola, 1964) X Classical taxonomy Corrêa and Espínola [86]
94 Psammolestes tertius (Lent & Jurberg, 1965) X Classical taxonomy Lent and Jurberg [87]
95 Triatoma sinica (Hsiao, 1965) X Classical taxonomy Hsiao [88]
96 Triatoma williami (Galvão et al., 1965) X Classical taxonomy Galvão et al. [89]
97 Triatoma bahiensis (Sherlock & Serafim, 1967) X Classical taxonomy Sherlock and Serafim [90]
98 Triatoma deaneorum (Galvão et al., 1967) X Classical taxonomy Galvão et al. [91]
99 Triatoma garciabesi (Carcavallo et al., 1967) X Classical taxonomy Carcavallo et al. [92]
100 Triatoma lenti (Sherlock & Serafim, 1967) X Classical taxonomy Sherlock and Serafim [90]
101 Panstrongylus lenti (Galvão & Palma, 1968) X Classical taxonomy Galvão and Palma [93]
102 Triatoma ryckmani (Zeledón & Ponce, 1972) X Classical taxonomy Zeledón and Ponce [94]
103 Rhodnius amazonicus (Almeida et al., 1973) X Classical taxonomy Almeida et al. [95]
104 Linshcosteusconfumus (Ghauri, 1976) X Classical taxonomy Ghauri [96]
105 Linshcosteuscostalis (Ghauri, 1976) X Classical taxonomy Ghauri [96]
106 Rhodnius dalessandroi (Carcavallo & Barreto, 1976) X Classical taxonomy Carcavallo and Barreto [97]
107 Alberproseniagoyovargasi (Martínez & Carcavallo, 1977) X Classical taxonomy Martínez and Carcavallo [98]
108 Rhodnius paraensis (Sherlock et al., 1977) X Classical taxonomy Sherlock et al. [99]
109 Triatoma cavernicola (Else & Cheong, 1977) X Classical taxonomy Else et al. [100]
110 Belminus herreri (Lent & Wygodzinsky, 1979) X Classical taxonomy Lent and Wygodzinsky [101]
111 Linshcosteuschota (Lent & Wygodzinsky, 1979) X Classical taxonomy Lent and Wygodzinsky [101]
112 Linshcosteuskali (Lent & Wygodzinsky, 1979) X Classical taxonomy Lent and Wygodzinsky [101]
113 Microtriatoma borbai (Lent & Wygodzinsky, 1979) X Classical taxonomy Lent and Wygodzinsky [101]
114 Parabelminus yurupucu (Lent & Wygodzinsky, 1979) X Classical taxonomy Lent and Wygodzinsky [101]
115 Triatoma guazu (Lent & Wygodzinsky, 1979) X Classical taxonomy Lent and Wygodzinsky [101]
116 Alberproseniamalheiroi (Serra et al., 1980) X Classical taxonomy Serra et al. [102]
117 Triatoma brailovskyi (Martínez et al., 1984) X Classical taxonomy Martínez et al. [103]
118 Cavernicola lenti (Barrett & Arias, 1985) X Classical taxonomy Barrett and Arias [104]
119 Triatoma bolivari (Carcavallo et al., 1987) X Classical taxonomy Carcavallo et al. [105]
120 Hermanlentia matsunoi (Fernández-Loayza, 1989) X Classical taxonomy Fernández-Loayza [106]
121 Rhodnius stali (Lent et al., 1993) X Classical taxonomy Lent et al. [107]
122 Belminus pittieri (Osuna & Ayala, 1993) X Classical taxonomy Osuna and Ayala [108]
123 Triatoma gomeznunezi (Martínez et al., 1994) X Classical taxonomy Martínez et al. [109]
124 Belminus laportei (Lent et al., 1995) X Classical taxonomy Lent et al. [110]
125 Mepraia gajardoi (Frias et al., 1998) X X X Integrative taxonomy Frias et al. [111]
126 Triatoma carcavalloi (Jurberg et al., 1998) X Classical taxonomy Jurberg et al. [112]
127 Triatoma jurbergi (Carcavallo et al., 1998) X Classical taxonomy Carcavallo et al. [113]
128 Triatoma bassolsae (Alejandre Aguilar et al., 1999) X Classical taxonomy Aguilar et al. [114]
129 Rhodnius colombiensis (Mejia et al., 1999) X Classical taxonomy Mejia et al. [115]
130 Triatoma baratai (Carcavallo & Jurberg, 2000) X Classical taxonomy Carcavallo and Jurberg [116]
131 Rhodnius milesi (Carcavallo et al., 2001) X Classical taxonomy Valente et al. [117]
132 Triatoma klugi (Carcavallo et al., 2001) X Classical taxonomy Carcavallo et al. [118]
133 Linshcosteuskarupus (Galvão et al., 2002) X Classical taxonomy Galvão et al. [119]
134 Triatoma sherlocki (Papa et al., 2002) X Classical taxonomy Papa et al. [120]
135 Triatoma vandae (Carcavallo et al., 2002) X Classical taxonomy Carcavallo [121]
136 Triatoma dominicana (Ponair Jr., 2005) X Classical taxonomy Ponair Jr. [122]
137 Belminus corredori (Galvão & Angulo, 2006) X Classical taxonomy Galvão and Ângulo [123]
138 Belminus ferroae (Sandoval et al., 2007) X Classical taxonomy Sandoval et al. [124]
139 Panstrongylus mitarakaensis (Bérenger & Blanchet, 2007) X Classical taxonomy Bérenger and Blanchet [125]
140 Triatoma boliviana (Martinez et al., 2007) X Classical taxonomy Martinez et al. [126]
141 Triatoma juazeirensis (Costa & Felix, 2007) X Classical taxonomy Costa and Felix [127]
142 Panstrongylus martinezorum (Ayala, 2009) X Classical taxonomy Ayala [128]
143 Rhodnius zeledoni (Jurberg et al., 2009) X Classical taxonomy Jurberg et al. [129]
144 Mepraia parapatrica (Frías-Lasserre, 2010) X X Integrative taxonomy Frías-Lasserre [12]
145 Rhodnius montenegrensis (Rosa et al., 2012) X X Integrative taxonomy Rosa et al. [13]
146 Panstrongylus hispaniolae (Ponair Jr., 2013) X Classical taxonomy Ponair Jr. [130]
147 Rhodnius barretti (Abad-Franch et al., 2013) X X Integrative taxonomy Abad-Franch et al. [14]
148 Triatoma jatai (Gonçalves et al., 2013) X Classical taxonomy Gonçalves et al. [131]
149 Triatoma pintodiasi (Jurberg et al., 2013) X X Integrative taxonomy Jurberg et al. [11]
150 Rhodnius marabaensis (Souza et al., 2017) X X Integrative taxonomy Souza et al. [15]
151 Nesotriatoma confusa (Oliveira et al., 2018) X Classical taxonomy Oliveira et al. [132]
152 Triatoma mopan (Dorn et al., 2018) X X Integrative taxonomy Dorn et al. [16]
153 Paleotriatoma metaxytaxa (Poinar Jr., 2019 ) X Classical taxonomy Poinar Jr. [133]
154 Triatoma huehuetenanguensis (Lima-Cordon et al., 2019) X X Integrative taxonomy Lima-Cordon et al. [17]
155 Triatoma rosai (Alevi et al., 2020) X X X X X Integrative taxonomy Alevi et al. [5]
156 Rhodnius micki (Zhao et al., 2021) X Classical taxonomy Zhao et al. [6]
157 Belminus santosmalletae (Dale et al., 2021) X Classical taxonomy Dale et al. [7]
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More than 190 synonymization acts occurred in the subfamily Triatominae [18,19], with the majority of synonymized taxa being described from classical taxonomy. The use of combined analyses for the characterization of a taxon greatly reduces the chances of synonymization (although it does not make it impossible [19,20]). Based on the synonymization events and the importance of multi-analyses for the characterization of a taxon, we will discuss the current issues, applications, and limitations of classical, molecular, and integrative taxonomy.

2.1. Classical Taxonomy

Classical taxonomy underlies most taxonomic studies of species description in the subfamily Triatominae (Table 2). The morphological and morphometric studies applied in the last described taxa are: morphological study of the head, thorax, abdomen, and male and female genitalia (with optical microscopy (OM) and/or scanning electronic microscopy (SEM)), and morphometric study of the head, thorax, abdomen and appendices (using OM) [5,6,7,15,16,17,132].

Although the use of morphological and morphometric characters is essential to describe a new taxon (since the diagnosis of the species needs to be made based on specimens that will be deposited, such as vouchers, in entomological collections), evolutionary events of cryptic speciation [14] and phenotypic plasticity [14] present in the subfamily Triatominae can make it difficult to diagnose a taxon only by morphological studies. Classic examples of this can be seen in the genus Rhodnius Stål, 1859: R. montenegrensis Rosa et al., 2012 [13] and R. marabaensis Souza et al., 2017 [15] represent two of the four paraphyletic strains of R. robustus Larrousse, 1927 [134,135] (the application of integrative taxonomy allowed description of the species from specimens initially characterized as R. robustus [136]). On the other hand, was demonstrated that R. taquarussiensis Rosa et al., 2017 (species described by integrative taxonomy [20]) represented only an intraspecific polymorphism of R. neglectus Lent, 1954 [19] (from studies of molecular taxonomy combined with experimental crosses it was possible to synonymize the species [19]).

Morphological convergence events can also hinder the classic taxonomy of these vectors [129]. The paraphyletic genus Triatoma Laporte, 1832 needs several studies from a taxonomic and systematic point of view [137]. Triatoma tibiamaculata (Pinto, 1926), for example, is a species that has morphological characteristics that bring it together and groups it (until now) as a Triatoma [138]. However, the generic status of this vector has been questioned several times [134,137,138]—since it presents cytogenetic [139], structural [140] and phylogenetic [137,138] characteristics that bring it closer to Panstrongylus (which highlights the importance of studies with integrative taxonomy).

2.2. Molecular Taxonomy

The first phylogenetic trees with molecular markers were published only in 1998 [141], giving rise to the phylogenetic systematics and molecular taxonomy of these vectors. Although no species of triatomine has been described by molecular taxonomy (Table 2), the combination of phylogenetic analyses with morphological and morphometric studies in species description studies (integrative taxonomy) has been a trend in the last decade [5,13,14,15,16,17] (Table 2), since it provides greater reliability of the specific status of the taxa and allows, above all, to understand the evolutionary history of the species.

In addition to the contributions mentioned above, molecular taxonomy and phylogenetic systematics allowed the evaluation and re-validation of the taxonomic status of some species: reinclusion of Linshcosteus Distant, 1904 genus in Triatomini tribe (extinguishing the Linshcosteini tribe) [30]; inclusion of Psammolestes Bergroth, 1911 species in the genus Rhodnius [30] (proposal not accepted by the scientific community due to the differences that support the generic status of Psammolestes [17]); inclusion of the species T. flavida Neiva, 1911, and N. obscura Maldonado & Farr, 1962 in the genus Nesotriatoma Usinger, 1944 [142]; confirmation of the generic status of Nesotriatoma [132]; inclusion of species T. spinolai Porter, 1934, M. gajardoi Frias, Henry & Gonzalez, 1998, T. eratyrusiformis Del Ponte, 1929, and T. breyeri Del Ponte, 1929 in the genus Mepraia Mazza, Gajardo & Jörg, 1940 [142] (partially accepted suggestion, being the Mepraia genus currently composed of M. spinolai, M. gajardoi, and M. parapatrica Frías-Lasserre, 2010 [4,143]); confirmation of the generic status of Mepraia [137]; and inclusion of T. dimidiata (Latreille, 1811) in the Meccus Stål, 1859 genus (genus that later was considered invalid and the Meccus species started to be considered as Triatoma [137,144,145]).

Although the International Code of Zoological Nomenclature does not consider groupings of triatomines to be complexes or subcomplexes [146], Justi et al. [137] suggests that these groupings should represent monophyletic groups. In the genus Triatoma, for example, studies based on phylogenetic systematics evaluated the position of several species that had been grouped mainly by geographic distribution and morphological similarities and proposed regrouping and/or the creation of new monophyletic groups [137,147,148]. Species well defined as natural groups (monophyletic) are currently the T. brasiliensis [149,150], T. sordida [151], T. rubrovaria [151], T. infestans [137], and T. vitticeps [148] subcomplexes.

2.3. Integrative Taxonomy

The data integration in the integrative taxonomy can be done by cumulation or congruence [152]. The use of combined tools to delimit a species of triatomine occurred for the first time in 1998 by Frias et al. [111] who combined morphological, morphometric, cytogenetic, and reproductive barriers data to describe M. gajardoi (Table 2). However, only in the last decade has the integrative taxonomy has been more applied in the study of these vectors (Table 2).

This tendency to integrate different analyses to characterize a taxon, made it possible to resolve ancient taxonomic issues, such as the description by T. mopan Dorn et al. (2018) and T. huehuetenanguensis Lima-Cordón et al. (2019) from specimens initially characterized as T. dimidiata [16,17,153,154] and the recent description of T. rosai Alevi et al., 2020 from the allopatric population of T. sordida (Stål, 1859) from Argentina [5,155,156]. In addition, the specific status of T. bahiensis Sherlock & Serafim, 1967 (a species that for more than three decades has been synonymous with T. lenti Sherlock & Serafim, 1967 [101]) has been revalidated based on integrative taxonomy [149].

On the other hand, even if the integrative taxonomy provides more robustness in the characterization of the new taxa (decreasing the chance of synonymization), does not prevent this event can occur (as mentioned above for R. taquarussuensis which has been synonymous with R. neglectus Lent, 1954 [19]). Although morphological, morphometric, and cytogenetic intraspecific variation had been described in the genus Rhodnius [157,158], the description of R. taquarussuensis was based on these factors [20]. Thus, synonymization event occurred through phylogenetic analyses and experimental crosses [19]. We suggest that integrative taxonomy work should include molecular studies and, whenever possible, reproductive barriers to confirm the taxon specific status following the biological concept of species [159,160,161].

In general, most articles of description based on integrative taxonomy combine only morphological and morphometric data with molecular analyses (Table 2). However, it is worth mentioning that in 2020 the description of T. rosai was published based on morphometric, morphological, molecular data, and experimental crosses that have been combined with information from the literature about the species (cytogenetic data [155,156], electrophoresis pattern [155], cuticular hydrocarbons pattern [162], geometric morphometry [163], cycle, and average time of life [164,165,166] as well as geographic distribution [18,42,43,44,50,51]), becoming the most complete article of species description of the subfamily Triatominae [5].

3. Overview of Tools Applied to Taxonomic Studies of Triatomines

In addition to species descriptions, several taxonomic studies have been carried out to assess the specific status of valid species and, above all, to assist in the correct classification of Chagas disease vectors. Based on this, we will specifically discuss the application of each taxonomic tool.

3.1. Morphology and Comparative Morphology

As already mentioned above, morphological studies are applied to all formal species descriptions (Table 2). These analyses can characterize several structures that, in general, are compared and confirm the specific status of triatomines [5,6,11,12,13,14,15,16,17]. Studies with OM and SEM allow characterizing structures of the head, thorax, and abdomen. These analyses are very important for classical taxonomy and support the main dichotomous keys used for the correct identification of these vectors [101,167,168,169,170,171,172].

3.2. Morphometry

Like morphological studies, morphometric studies are also present in the description of all triatomines (at first, showing the size of specimens and structures and, later, by means of geometric morphometry [4]). These measurable data are very important from a taxonomic point of view, as a visual identification system was recently developed from morphometric data that has the potential to automate the identification of triatomines [173,174].

3.3. Chemotaxonomy

In 1964, Actis et al. [175] used, for the first time, biochemical studies with hemolymph protein electrophoresis to compare species of triatomines, giving rise to chemotaxonomy. Isoenzymes were applied to different species of Rhodnius [176], the T. brasiliensis subcomplex [177] and Mexican Triatoma [178]. However, recently, biochemical studies are rare from a taxonomic perspective; they contribute to the integrative taxonomy as shown by Jurberg et al. [11] and Alevi et al. [5] with the species descriptions of T. pintodiasi Jurberg et al., 2013 and T. rosai respectively.

3.4. Cytotaxonomy and Karyosystematic

Cytotaxonomy was started with Ueshima [179] by proposing the application of cytogenetic studies of chromosomes to differentiate morphologically related species. Later, the use of chromosomal analyses—such as karyotypes [180,181,182,183]—the constitutive heterochromatin pattern [156,184,185], the heterochromatin base pair composition [186,187,188], and the location of the nucleolar organizing region [139,156,189], assisted in the correct identification and classification of triatomines. Recently, dichotomous keys have been proposed based on cytogenetic data [190,191,192,193].

3.5. MALDI-TOF MS

Laroche et al. [194] used, for the first time, matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) analysis to differentiate triatomine species. The researchers were able to differentiate species from French Guiana by MALDI-TOF. Subsequently, Souza et al. [195] used these analyses to differentiate 12 species of the genus Rhodnius. Furthermore, Souza et al. [196] also differentiated the species of Cavernicola Barber, 1937.

3.6. Omics

In 2017, omics tools (transcriptomics) were used for the first time in taxonomic studies of triatomines to confirm the specific status of R. montenegrensis [197]. In 2019, Brito et al. [198] also validated the specific status of R. montenegrensis and confirmed that this species refers to strain II of the paraphyletic group of R. robustus.

4. Concluding Remarks

Classical taxonomy, over the last few decades, has been revitalized by integrative taxonomy leading to success in the identification and delimitation of new species through the use of multiple and complementary approaches. Most descriptions of triatomine species are based on classical taxonomy. Facing evolutionary (cryptic speciation and phenotypic plasticity) and taxonomic (more than 190 synonymizations) problems has indicated that it is evident that integrative taxonomy studies are an important and necessary trend for this group of vectors. However, from the synonymization of R. taquarussuensis (which was described through integrative taxonomy [20] and was later synonymized with R. neglectus [19]), it is evident that phylogenetic studies (molecular taxonomy) should be considered among the analyses used for the description of new species from the integrative taxonomy (Figure 1).

Figure 1.

Figure 1

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Schematic representation of the integrative taxonomy of triatomines.

Author Contributions

Conceptualization, K.C.C.A., J.d.O., D.d.S.R. and C.G.; Writing—original draft preparation, K.C.C.A., J.d.O., D.d.S.R. and C.G.; Writing—review and editing, K.C.C.A., J.d.O., D.d.S.R. and C.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by São Paulo Research Foundation, Brazil (FAPESP) (Process number 2017/05015-7 and 2019/02145-2), the Coordination for the Improvement of Higher Education Personnel, Brazil (CAPES)—Finance Code 001 and the National Council for Scientific and Technological Development, Brazil (CNPq).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All relevant data are within the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

Footnotes

Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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