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Article

Revisiting the Genetic, Taxonomic and Evolutionary Aspects of Chagas Disease Vectors of the Triatoma phyllosoma Subcomplex (Hemiptera, Triatominae)

by
Natália Regina Cesaretto
1,†,
Yago Visinho dos Reis
1,†,
Jader de Oliveira
2,
Cleber Galvão
3,* and
Kaio Cesar Chaboli Alevi
1,2,3
1
Instituto de Biociências de Botucatu, Universidade Estadual Paulista “Júlio de Mesquita Filho” (UNESP), Rua Dr. Antônio Celso Wagner Zanin, 250, Distrito de Rubião Junior, Botucatu 18618-689, SP, Brazil
2
Laboratório de Entomologia em Saúde Pública, Faculdade de Saúde Pública, Universidade de São Paulo (USP), Av. Dr. Arnaldo 715, São Paulo 01246-904, SP, Brazil
3
Laboratório Nacional e Internacional de Referência em Taxonomia de Triatomíneos, Instituto Oswaldo Cruz (FIOCRUZ), Av. Brasil 4365, Pavilhão Rocha Lima, Sala 505, Rio de Janeiro 21040-360, RJ, Brazil
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Diversity 2022, 14(11), 978; https://doi.org/10.3390/d14110978
Submission received: 29 September 2022 / Revised: 3 November 2022 / Accepted: 3 November 2022 / Published: 14 November 2022
(This article belongs to the Special Issue Heteroptera: Biodiversity, Evolution, Taxonomy and Conservation)
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Abstract

:
Triatoma bassolsae, T. longipennis, T. mazzottii, T. pallidipennis, T. phyllosoma and T. picturata are species that have great epidemiological importance in the transmission of Chagas disease in Mexico. However, there is no consensus regarding the specific status of these species, since they appear in various articles as species, subspecies and even subgenera. Thus, we revisited genetic, taxonomic and evolutionary data that allowed us to assess and discuss the specific status of these six species of the T. phyllosoma subcomplex. Phylogenetic studies were performed with nuclear (18S, 28S, ITS-2) and mitochondrial (16S, cytb, COI, COII, 12S) markers deposited in GenBank. In addition, data from experimental crosses were pooled and the genetic distance to the cytb gene was calculated. The phylogenetic reconstruction enabled us to rescue the six species as independent lineages. Post-zygotic reproductive isolation barriers (sterility and/or hybrid collapse) were observed for some experimental crosses. Although the other experimental crosses did not allow us to characterize reproductive barriers, these species showed high genetic distances in relation to the cytb gene (ranging from 4.6% to 14.9%). Thus, based on the revisited literature data, we confirmed the specific status of these six species of the T. phyllosoma subcomplex based on the phylogenetic and biological concepts of the species.

1. Introduction

The Chagas disease vectors of the Triatomini tribe (Hemiptera, Triatominae) have been grouped into eight complexes and nine subcomplexes (Figure 1) [1,2,3,4,5]. Although these groupings are not recognized by the International Code of Zoological Nomenclature [6], it has been suggested that they should represent natural groups (monophyletic) [7]. The Triatoma phyllosoma subcomplex is composed of the species T. bassolsae Alejandre Aguilar et al., 1999; T. bolivari Carcavallo, Martínez and Pelaez, 1987; T. longipennis (Usinger, 1939); T. mazzottii (Usinger, 1941); T. mexicana (Herrich-Schaeffer, 1848); T. pallidipennis (Stål, 1872); T. phyllosoma (Burmeister, 1835); T. picturata (Usinger, 1939) and T. ryckmani Zeledón and Ponce, 1972 [1]. With the exception of T. ryckmani, all the species of the T. phyllosoma subcomplex are endemic to Mexico [8].
Triatoma bassolsae, T. longipennis, T. mazzottii, T. pallidipennis, T. phyllosoma and T. picturata are species that have great epidemiological importance in the transmission of Chagas disease in Mexico, representing more than 60% of vectorial transmissions of Trypanosoma cruzi (Chagas, 1909) (Kinetoplastida, Trypanosomatidae) to humans [9]. In addition to their epidemiological importance, these insects have a complex taxonomy, since they were once considered a single species with genetic and morphological polymorphism and/or subspecies of T. phyllosoma [10].
Triatoma bassolsae was described in 1999 as a species of the genus Triatoma Laporte, 1832 [11]. In 2000, Carcavallo et al. [12] suggested the reclassification of the species to the genus Meccus Stål, 1859, and recently Justi et al. [7] and Cesaretto et al. [13] demonstrated that it is a species of Triatoma. Triatoma longipennis was described 1939 as a species of the genus Triatoma [14]. In 1944, it was considered as a subspecies: T. p. longipennis [15]. In 2000, Carcavallo et al. [12] suggested that the subspecies was a species and grouped it into the genus Meccus. Recently it was demonstrated that this species belongs to the genus Triatoma [7,13]. Triatoma mazzottii was described 1941 as a species of the genus Triatoma [16]. In 1943/1944, it was considered a subspecies (T. p. mazzottii) [15,17]. Later, it came to be considered as a species and was classified in the genus Meccus [12] and recently it has been regrouped into the genus Triatoma [7,13].
Triatoma pallidipennis was described in 1872 as a species of the genus Triatoma [18]. In 1943/1944, it was considered a subspecies (T. p. pallidipennis) [15,17]. In 2000, it started to be considered a species and was placed in the genus Meccus [12]. Recently Justi et al. [7] and Cesaretto et al. [13] demonstrated that it is a speciesof Triatoma. Triatoma phyllosoma was described in 1835 as a species of the genus Conorhinus [19]. In 1930, it came to be considered a species of the genus Triatoma [20]. In 2000, it was classified in the genus Meccus [12] and recently it has been regrouped into the genus Triatoma [7,13]. Finally, T. picturata was described in 1939 as a species of the genus Triatoma [14]. In 1943/1944, it was considered a subspecies (T. p. picturata) [15,17]. In 2000, Carcavallo et al. [12] suggested that the subspecies was a species and grouped it into the genus Meccus. Recently it was demonstrated that this species belongs to the genus Triatoma [7,13].
As demonstrated above, the generic status of the T. phyllosoma subcomplex species has also been widely discussed. The first species of this genus was described as Conorhinus phyllosoma Burmeister, 1835 [19]; in 1859 the species was transferred to the genus Meccus [20]; in 1930 it was transferred to the genus Triatoma [21]; in 2000 the genus Meccus was revalidated based on morphological data [12] (alteration corroborated by Hypsa et al. [22] through molecular studies); and in 2014 the genus Meccus was synonymized with Triatoma using more sophisticated phylogenetic reconstruction methods [7] (generic alteration recently confirmed by experimental crosses [13]).
Recently, Rengifo-Correa et al. [23] proposed an identification key for the T. phyllosoma species group (involving species of the T. phyllosoma and T. dimidiata subcomplexes) and suggested that T. bassolsae, T. longipennis, T. mazzottii, T. pallidipennis, T. phyllosoma and T. picturata should be considered species. However, there is no consensus among researchers between the specific status of these species, since they appear in articles as species [23], subspecies [24,25] and even subgenera [26,27]. Thus, we revisited genetic, taxonomic and evolutionary data that allowed us to assess and discuss the specific status of these six species of the T. phyllosoma subcomplex.

2. Materials and Methods

Sequences of eight molecular markers obtained in GenBank (mitochondrial markers: 16S, cytb, COI, COII and 12S; nuclear markers: 18S, 28S and ITS-2) (Table 1) were used for the T. phyllosoma subcomplex species (T. bassolsae, T. longipennis, T. mazzottii, T. pallidipennis, T. phyllosoma and T. picturata) and for two Triatoma species (T. brasiliensis Neiva, 1911 and T. vitticeps (Stål, 1859)), which were designated as an outgroup (Table 1). The sequences were submitted to the MEGA X program [28] and aligned using the muscle method [29]. The alignments of each marker were concatenated by name using the Seaview4 program [30] and converted with the Mesquite program [31], resulting in an alignment with eight taxa and 5556 nucleotides.
The concatenated alignment was partitioned for each marker and the best nucleotide substitution model (lowest Akaike information criterion value) was individually determined in the jModelTest 2 program [32] (Table 1). Data were submitted to MrBayes 3.2 [33] for phylogenetic reconstruction using a Bayesian approach, with a total of 100 million generations. Trees were sampled every 1000 generations in two independent runs, with burn-in adjusted to 25%. The Tracer v. 1.7 program [34] was used to verify the stabilization (ESS values above 200) of the sampled trees and the generated phylogenetic tree was viewed and edited in the FigTree v.1.4.4 program [35], being rooted at the midpoint. A concatenated sequence tree was produced based on the mitochondrial and nuclear genes once the concatenation approach had yielded more accurate trees, even when the concatenated sequences had evolved with very different substitution patterns [36]. The genetic distance matrix between the T. phyllosoma subcomplex species was obtained in the MEGA X program 21 based on the cytb sequences (Table 2) using the Kimura 2-parameter distance model [37]. The use of only one specimen of each species in the matrix was justified because the objective of this genetic distance analysis was to assess the taxonomic status of each of the six taxa of this subcomplex (interspecific) and not to carry out population studies (intraspecific).

3. Results and Discussion

The phylogenetic reconstruction, obtained by combining different mitochondrial and nuclear markers, could be used to rescue the six species of the T. phyllosoma subcomplex as independent lineages with strong bootstrap values (values ≥ 70%) [38] (with support values ranging from 0.82 to 1) (Figure 2). In addition, these species showed high genetic distances from the cytb gene, ranging from 4.6% to 14.9% (Table 2).
Phylogenetic studies performed by Martinez-Ibarra et al. [10] and Martínez et al. [39] led those authors to propose changing the specific status of species T. bassolsae, T. longipennis, T. mazzottii, T. pallidipennis, T. phyllosoma and T. picturata to subspecies of T. phyllosoma (T. p. bassolsae, T. p. longipennis, T. p. mazzottii, T. p. pallidipennis, T. p. phyllosoma and T. p. picturata). However, the phylogenetic reconstruction obtained by combining different mitochondrial and nuclear markers enabled us to rescue the six species of the T. phyllosoma subcomplex as independent lineages (Figure 2), confirming the specific status of these vectors based on the phylogenetic concept of species (“… the smallest diagnosable cluster of individual organisms forming a monophyletic group within which there is a parental pattern of ancestry and descent” [40]).
Post-zygotic reproductive isolation barriers (sterility and/or hybrid collapse) that make the hybrids resulting from the crosses between T. mazzotti and most other species of the T. phyllosoma subcomplex unfeasible, as well as those between T. phyllosoma and T. pallidipennis and between T. phyllosoma and T. bassolsae, were described by Martinez-Ibarra [41,42,43] (Table 3). The characterization of these barriers under laboratory conditions confirmed the specific status of the parent species based on the biological species concept (“… groups of actually or potentially interbreeding natural populations, which are reproductively isolated from other such groups” [44,45]). Although the other experimental crosses did not allow the characterization of interspecific reproductive barriers (Table 3), these species showed high genetic distances from the cytb gene (the choice of the cytb gene to calculate the genetic distance was based on the minimum interspecific distance established by Monteiro et al. [46]), ranging from 4.6% to 14.9% (Table 2), which confirmed the specific status of all taxa, since these were greater than the minimum value established to separate species using the cytb gene (2%) [46].
Usinger [15] was the first researcher to question the specific status of T. longipennis, T. mazzottii, T. pallidipennis, T. phyllosoma and T. picturata, suggesting the shifting of T. phyllosoma from a species to subspecies (considering this species as polytypic). Lent and Wygodinsky [47], based on morphological data, elevated its status to a species. On the other hand, Marcilla et al. [48], Martínez et al. [39], Martinez-Ibarra et al. [10] and Bargues et al. [49] performed molecular studies and observed very low interspecific variations, suggesting that classifying the species as subspecies would be more appropriate. However, Renfigo-Correa et al. [23,50], based on the phenetics and cohesion species concept considered T. bassolsae, T. longipennis, T. mazzottii, T. pallidipennis, T. phyllosoma and T. picturata as valid species. These concepts suggest, respectively, that "a species is a set of organisms that are phenotypically similar and that look different from other sets of or-ganisms [51]" and "a species is an evolutionary lineage that serves as the arena of action of basic micro-evolutionary forces, such as gene flow—when applicable—genetic drift and natural selection [52]".
As mentioned above, although T. longipennis, T. pallidipennis and T. picturata live in sympatry and produce natural hybrids [10], there is some evolutionary factor that makes these hybrids unfeasible under natural conditions [which was not visualized under artificial conditions (Table 3)], since these taxa have a high interspecific genetic distance (Table 2), which demonstrates the genetic integrity of the three species, possibly resulting from reproductive isolation due to a post-zygotic barrier (a barrier that possibly inhibits the backcrossing and gene introgression between T. longipennis, T. pallidipennis and T. picturata under natural conditions).
Chagas disease is one of the most important yet neglected parasitic diseases in Mexico and is transmitted by Triatominae [53]. Nineteen of the 31 Mexican triatomine species are considered important species from an epidemiological point of view (including the six species studied here), as they invade human houses and all have been found to be naturally infected with T. cruzi [53]. The precise classification of T. bassolsae, T. longipennis, T. mazzottii, T. pallidipennis, T. phyllosoma and T. picturata species has epidemiological implications, as it allows vector control programs to direct monitoring and control activities directly to the species with the greatest vector importance.
These six species have interspecific morphological divergences that allow the species to be differentiated (also allowing the organization of dichotomous keys) [23,47]. Furthermore, the study of their external female genitalia [54] and the eggs [55] by means of scanning electron microscopy showed significant interspecific differences that allowed for the confirmation of the specific status of the species.

4. Conclusions

Thus, based on the literature data that were revisited and discussed here (morphological, genetic and evolutionary data), we confirmed the specific status of T. bassolsae, T. longipennis, T. mazzottii, T. pallidipennis, T. phyllosoma and T. picturata based on the phylogenetic, phenetic, cohesion and biological concepts of the species. Finally, we consider it important to carry out further studies to evaluate the presence/absence of interspecific gene flow (such as microsatellite markers and next-generation sequencing) between T. phyllosoma subcomplex species under natural conditions.

Author Contributions

Conceptualization, N.R.C., Y.V.d.R., J.d.O., C.G. and K.C.C.A.; methodology, N.R.C., Y.V.d.R., J.d.O., C.G. and K.C.C.A.; formal analysis, N.R.C., Y.V.d.R. and K.C.C.A.; investigation, N.R.C., Y.V.d.R. and K.C.C.A.; resources, J.d.O., C.G. and K.C.C.A.; writing—original draft preparation, N.R.C., Y.V.d.R. and K.C.C.A.; writing—review and editing, N.R.C., Y.V.d.R., J.d.O., C.G. and K.C.C.A.; supervision, J.d.O. and K.C.C.A.; project administration, N.R.C., J.d.O. and K.C.C.A.; funding acquisition, C.G. and K.C.C.A. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), Coordination for the Improvement of Higher Education Personnel, Brazil (CAPES)—Finance Code 001, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Carlos Chagas Filho Research Foundation of the State of Rio de Janeiro (FAPERJ).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

All relevant data are contained within the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Complexes and subcomplexes that are used to group the species of the Triatomini tribe. The shaded groupings represent species that have already been reported in Mexico.
Figure 1. Complexes and subcomplexes that are used to group the species of the Triatomini tribe. The shaded groupings represent species that have already been reported in Mexico.
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Figure 2. Bayesian phylogenetic tree. The posterior probability is indicated in the nodes.
Figure 2. Bayesian phylogenetic tree. The posterior probability is indicated in the nodes.
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Table
Table 1. GenBank access codes of sequences used in the molecular analysis of the T. phyllosoma subcomplex species and respective nucleotide substitution models. - represents genes that have not been sequenced.
Table 1. GenBank access codes of sequences used in the molecular analysis of the T. phyllosoma subcomplex species and respective nucleotide substitution models. - represents genes that have not been sequenced.
SpeciesMolecular Markers
(Substitution Models)
16S18S28SCytbCOICOIIITS-212S
(GTR + I + G)(HKY +I)(HKY)(HKY + G)(GTR + I)(HKY)(HKY)(GTR)
T. phyllosoma subcomplex
T. pallidipennisKC249045AJ243330-DQ198814--AJ286882AF394522
T. longipennisKC249031-KC249177KC249267KC249357KC249452KC698909-
T. mazzottiiAY035446AJ243333-DQ198816DQ198805-KC698911-
T. picturataAY035447AJ243332-DQ198817--KC698910-
T. phyllosoma-AJ243329-DQ198818DQ198806-KC698912-
T. bassolsae---MK317878--MK248256-
Outgroup
T. brasiliensisKC248985AJ421957KC249145KC249239KC249318KC249413-AF021187
T. vitticepsKC249087KC249132KC249220KC249303KC249396KC249491-AF021217
Table
Table 2. Genetic distance matrix for the cytochrome b gene.
Table 2. Genetic distance matrix for the cytochrome b gene.
Species12345678
1T. pallidipennis
2T. longipennis0.104
3T. mazzottii0.1360.102
4T. picturata0.0900.1060.148
5T. phyllosoma0.1240.0910.1220.147
6T. bassolsae0.0460.0990.1490.0840.132
7T. brasiliensis0.3150.2960.3260.3600.2760.336
8T. vitticeps0.2950.2670.2950.2650.2670.2560.302
Table
Table 3. Experimental crosses carried out between species of the phyllosoma subcomplex.
Table 3. Experimental crosses carried out between species of the phyllosoma subcomplex.
Experimental CrossesPre-Zygotic
Barriers		Post-Zygotic
Barriers		References
♀ T. mazzottii × ♂ T. longipennisAbsentHybrid CollapseMartínez-Ibarra et al. [41]
♂ T. mazzottii × ♀ T. longipennisAbsentHybrid CollapseMartínez-Ibarra et al. [41]
♀ T. mazzottii × ♂ T. picturataAbsentHybrid sterilityMartínez-Ibarra et al. [41]
♂ T. mazzottii × ♀ T. picturataAbsentHybrid sterilityMartínez-Ibarra et al. [41]
♀ T. mazzottii × ♂ T. pallidipennisAbsentHybrid sterilityMartínez-Ibarra et al. [41]
♂ T. mazzottii × ♀ T. pallidipennisAbsentHybrid sterilityMartínez-Ibarra et al. [41]
♀ T. mazzottii × ♂ T. bassolsaeAbsentHybrid sterilityMartínez-Ibarra et al. [41]
♀ T. phyllosoma × ♂ T. pallidipennisAbsentHybrid sterilityMartínez-Ibarra et al. [42]
♀ T. pallidipennis × ♂ T. phyllosomaAbsentHybrid sterilityMartínez-Ibarra et al. [42]
♀ T. phyllosoma × ♂ T. bassolsaeAbsentHybrid sterilityMartínez-Ibarra et al. [42]
♀ T. bassolsae × ♂ T. phyllosomaAbsentHybrid sterilityMartínez-Ibarra et al. [42]
♀ T. longipennis × ♂ T. picturataAbsentAbsentMartínez-Ibarra et al. [41]
♂ T. longipennis × ♀ T. picturataAbsentAbsentMartínez-Ibarra et al. [41]
♀ T. phyllosoma × ♂ T. longipennisAbsentAbsentMartínez-Ibarra et al. [42]
♀ T. longipennis × ♂ T. phyllosomaAbsentAbsentMartínez-Ibarra et al. [42]
♀ T. phyllosoma × ♂ T. picturataAbsentAbsentMartínez-Ibarra et al. [42]
♀ T. picturata × ♂ T. phyllosomaAbsentAbsentMartínez-Ibarra et al. [42]
♀ T. phyllosoma × ♂ T. mazzottiiAbsentAbsentMartínez-Ibarra et al. [42]
♀ T. mazzottii × ♂ T. phyllosomaAbsentAbsentMartínez-Ibarra et al. [42]
♀ T. bassolsae × ♂ T. pallidipennisAbsentAbsentMartínez-Ibarra et al. [42]
♀ T. pallidipennis × ♂ T. bassolsaeAbsentAbsentMartínez-Ibarra et al. [42]
♀ T. bassolsae × ♂ T. longipennisAbsentAbsentMartínez-Ibarra et al. [42]
♀ T. longipennis × ♂ T. bassolsaeAbsentAbsentMartínez-Ibarra et al. [42]
♀ T. bassolsae × ♂ T. picturataAbsentAbsentMartínez-Ibarra et al. [42]
♀ T. picturata × ♂ T. bassolsaeAbsentAbsentMartínez-Ibarra et al. [42]
♀ T. longipennis × ♂ T. pallidipennisAbsentAbsentMartínez-Ibarra et al. [43]
♀ T. pallidipennis × ♂ T. longipennisAbsentAbsentMartínez-Ibarra et al. [43]
♀ T. pallidipennis × ♂ T. picturataAbsentAbsentMartínez-Ibarra et al. [43]
♀ T. picturata × ♂ T. pallidipennisAbsentAbsentMartínez-Ibarra et al. [43]
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Cesaretto, N.R.; dos Reis, Y.V.; de Oliveira, J.; Galvão, C.; Alevi, K.C.C. Revisiting the Genetic, Taxonomic and Evolutionary Aspects of Chagas Disease Vectors of the Triatoma phyllosoma Subcomplex (Hemiptera, Triatominae). Diversity 2022, 14, 978. https://doi.org/10.3390/d14110978

AMA Style

Cesaretto NR, dos Reis YV, de Oliveira J, Galvão C, Alevi KCC. Revisiting the Genetic, Taxonomic and Evolutionary Aspects of Chagas Disease Vectors of the Triatoma phyllosoma Subcomplex (Hemiptera, Triatominae). Diversity. 2022; 14(11):978. https://doi.org/10.3390/d14110978

Chicago/Turabian Style

Cesaretto, Natália Regina, Yago Visinho dos Reis, Jader de Oliveira, Cleber Galvão, and Kaio Cesar Chaboli Alevi. 2022. "Revisiting the Genetic, Taxonomic and Evolutionary Aspects of Chagas Disease Vectors of the Triatoma phyllosoma Subcomplex (Hemiptera, Triatominae)" Diversity 14, no. 11: 978. https://doi.org/10.3390/d14110978

APA Style

Cesaretto, N. R., dos Reis, Y. V., de Oliveira, J., Galvão, C., & Alevi, K. C. C. (2022). Revisiting the Genetic, Taxonomic and Evolutionary Aspects of Chagas Disease Vectors of the Triatoma phyllosoma Subcomplex (Hemiptera, Triatominae). Diversity, 14(11), 978. https://doi.org/10.3390/d14110978

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