Trends in taxonomy of Triatomini (Hemiptera, Reduviidae, Triatominae): reproductive compatibility reinforces the synonymization of Meccus Stål, 1859 with Triatoma Laporte, 1832
Parasites & Vectors volume 14, Article number: 340 (2021)
Meccus' taxonomy has been quite complex since the first species of this genus was described by Burmeister in 1835 as Conorhinus phyllosoma. In 1859 the species was transferred to the genus Meccus and in 1930 to Triatoma. However, in the twentieth century, the Meccus genus was revalidated (alteration corroborated by molecular studies) and, in the twenty-first century, through a comprehensive study including more sophisticated phylogenetic reconstruction methods, Meccus was again synonymous with Triatoma. Events of natural hybridization with production of fertile offspring have already been reported among sympatric species of the T. phyllosoma subcomplex, and experimental crosses demonstrated reproductive viability among practically all species of the T. phyllosoma subcomplex that were considered as belonging to the genus Meccus, as well as between these species and species of Triatoma. Based on the above, we carried out experimental crosses between T. longipennis (considered M. longipennis in some literature) and T. mopan (always considered as belonging to Triatoma) to evaluate the reproductive compatibility between species of the T. phyllosoma complex. In addition, we have grouped our results with information from the literature regarding crosses between species that were grouped in the genus Meccus with Triatoma, in order to discuss the importance of experimental crosses to confirm the generic reorganization of species.
The crosses between T. mopan female and T. longipennis male resulted in viable offspring. The hatching of hybrids, even if only in one direction and/or at low frequency, demonstrates reproductive compatibility and homeology between the genomes of the parents.
Considering that intergeneric crosses usually do not result in viable offspring in Triatominae, the reproductive compatibility observed between the T. phyllosoma subcomplex species considered in the Meccus genus with species of the Triatoma genus shows that there is “intergeneric” genomic compatibility, which corroborates the generic reorganization of Meccus in Triatoma.
Triatomines are hematophagous insects of great importance for public health, since they are considered the main form of transmission of the protozoan Trypanosoma cruzi (Chagas, 1909) (Kinetoplastida, Trypanosomatidae), the etiological agent of Chagas disease . Currently, there are 8 million infected people worldwide and around 25 million living in an area at risk of infection , the control of vector populations being the main measure for the reduction of new chagasic patients .
Triatomines are part of the Hemiptera order, Heteroptera suborder, Reduviidae family and Triatominae subfamily . There are 156 species in this subfamily, distributed in 18 genera and five tribes [3,4,5,6]. The Triatomini tribe is composed of nine genera, namely, Dipetalogaster Usinger, 1939, Eratyrus Stål, 1859, Hermanlentia Jurberg & Galvão, 1997, Linshcosteus Distant, 1904, Mepraia Mazza, Gajardo & Jörg, 1940, Nesotriatoma Usinger, 1944, Panstrongylus Berg, 1879, Paratriatoma Barber, 1938, and Triatoma Laporte, 1832 [3, 4]. However, during the taxonomic history within this tribe, several genera have already been considered valid: Eutriatoma Pinto, 1926, Conorhinus Laporte, 1833, Callotriatoma Usinger, 1939, Cenaeus Pinto, 1925, Neotriatoma Pinto, 1931, Lamus Stål, 1859, Mestor Kirkaldy, 1904, Triatomaptera Neiva & Lent, 1940, and Meccus Stål, 1859 [7, 8]. Eutriatoma, Conorhinus, Neotriatoma and Meccus were the genera synonymous with Triatoma [7, 8].
Meccus’ taxonomy has been quite complex, since the first species of this genus was described by Burmeister  as Conorhinus phyllosoma Burmeister, 1835; in 1859 the species was transferred to the genus Meccus  and in 1930 to Triatoma . However, in the twentieth century, Carcavallo et al.  proposed the revalidation of the Meccus genus based on morphological data (alteration corroborated by Hypsa et al.  through molecular studies). Finally, in the twenty-first century, Justi et al. , through a comprehensive study including more sophisticated phylogenetic reconstruction methods, again synonymized Meccus with Triatoma.
The six species initially considered as Meccus [T. bassolsae Aguilar, Torres, Jiménez, Jurberg, Galvão & Carcavallo, 1999, T. longipennis Usinger, 1939, T. mazzottii Usinger, 1941, T. pallidipennis Stål, 1872, T. phyllosomus (Burmeister, 1835), and T. picturatus Usinger, 1939], together with T. bolivari Carcavallo, Martínez & Pelaez, 1987, T. mexicana (Herrich-Schaeffer, 1848) and T. ryckmani Zeledón & Ponce, 1972, form the T. phyllosoma subcomplex . This subcomplex, together with the T. dimidiata subcomplex [T. dimidiata (Latreille, 1811), T. hegneri Mazzotti, 1940, T. huehuetenanguensis Lima-Cordón et al., 2019, T. mopan Dorn et al., 2018, T. brailovskyi Martínez, Carcavallo & Pelaez, 1984, and T. gomeznunezi Martínez, Carcavallo & Jurberg, 1994], form the T. phyllosoma complex [3, 14, 15].
Events of natural hybridization with production of fertile offspring have already been reported among sympatric species of the T. phyllosoma subcomplex . Experimental crosses demonstrated reproductive viability among practically all species of the T. phyllosoma subcomplex that were considered as belonging to genus Meccus in some literature [17, 18]. In addition, experimental crosses between these species and species of Triatoma from the T. phyllosoma subcomplex (T. mexicana) and the T. lecticularia complex [T. recurva (Stål, 1868)] also resulted in the production of hybrids [19, 20].
The study of reproductive barriers by experimental crossings was used in taxonomy (with emphasis on description, revalidation, and synonymization of species [5, 21, 22]) and systematics (with emphasis on the evolutionary relationship between species ) of Triatominae. Based on the above, we carried out experimental crosses between Triatoma species of the T. phyllosoma (T. longipennis) and T. dimidiata (T. mopan) subcomplexes, to evaluate the reproductive compatibility between species of the T. phyllosoma complex. In addition, we have grouped our results with information from the literature regarding crosses between species that were initially grouped in the genus Meccus with Triatoma, in order to discuss the importance of experimental crosses to confirm the generic reorganization of species.
Reciprocal experimental crosses were conducted between T. longipennis and T. mopan. These two species were chosen because both belong to the T. phyllosoma complex [3, 14, 15], and T. mopan has never been considered as belonging to Meccus, unlike T. longipennis. The insects used in the experiment came from colonies kept in the Triatominae insectary of the School of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, São Paulo, Brazil. The experimental crosses were conducted in the Triatominae insectary, according to the experiments of Correia et al.  and Mendonça et al. : the insects were sexed as fifth instar nymphs, and males and females were kept separately until they reached the adult stage to guarantee the virginity of the insects used in the crosses. For the experimental crosses, three couples from each set were placed in plastic jars (diameter 5 cm × height 10 cm) and kept at room temperature.
Results and discussion
As observed for the crosses between T. recurva and T. phyllosoma (as M. phyllosomus)  and between T. mexicana and T. longipennis , only the direction between T. mopan female and T. longipennis male resulted in viable offspring (Table 1). The hatching of hybrids, even if only in one direction and/or at low frequency (Table 1), demonstrates reproductive compatibility and homeology between the genomes of the parents.
Intergeneric crosses usually do not result in viable offspring in Triatominae (possibly due to pre-zygotic barriers, such as genomic incompatibility), as noted for the crossings between Panstrongylus and Triatoma, Panstrongylus and Nesotriatoma, Rhodnius Stål, 1859 and Psammolestes Bergroth, 1911 (KCCA, personal communication) and Rhodnius and Triatoma . The reproductive compatibility observed between the T. phyllosoma subcomplex species considered in the Meccus genus with species of the Triatoma genus (Table 1) shows that there is “intergeneric” genomic compatibility, which corroborates the regrouping of species in the same genus carried out by Justi et al. .
The genus Triatoma is a paraphyletic group comprising 82 species [3, 5, 8]. There are species of Triatoma related phylogenetically to the genera Panstrongylus, Paratriatoma, Linshcosteus and Hermanlentia , which justifies the paraphyly of the genus. The inclusion of the species of the genus Meccus in Triatoma rescues a discussion about the application of the morphological characteristics used for a long time as diagnoses for the genera of the subfamily Triatominae (as recently highlighted by Monteiro et al. ).
Taxonomy is a fundamental science for the entomo-epidemiology of Chagas disease, because correctly classifying triatomines can assist in the activity of vector control programs . Even though since 2014 the generic status of the species grouped in Meccus has been changed to Triatoma, several authors continued publishing articles using the Meccus nomenclature as valid [20, 29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46] and, quite mistakenly, as Triatoma (Meccus) pallidipennis [47,48,49]—since Meccus after the genus Triatoma (between parentheses) represents a subgenus and, so far, there are no valid subgenera in the subfamily Triatominae.
Thus, through reproductive compatibility, we confirm the generic reorganization of Meccus in Triatoma proposed by Justi et al. . In addition, we highlight the importance of the correct classification of the species of the T. phyllosoma subcomplex into this genus to avoid future misunderstandings by the scientific community and vector control programs.
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The data supporting the conclusions of this article are included within the article.
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We appreciate the à Pesquisa do Estado de São Paulo (FAPESP, Brazil), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil) – Finance Code 001, and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil) for financial support.
The study was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Brazil), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil) – Finance Code 001, and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil). JAR: CNPq, PQ-2, process 307 398/2018–8.
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Cesaretto, N.R., de Oliveira, J., Ravazi, A. et al. Trends in taxonomy of Triatomini (Hemiptera, Reduviidae, Triatominae): reproductive compatibility reinforces the synonymization of Meccus Stål, 1859 with Triatoma Laporte, 1832. Parasites Vectors 14, 340 (2021). https://doi.org/10.1186/s13071-021-04847-7