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Trends in Evolution of the Rhodniini Tribe (Hemiptera, Triatominae): Experimental Crosses Between Psammolestes Tertius Lent &

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Trends in Evolution of the Rhodniini Tribe (Hemiptera, Triatominae): Experimental Crosses Between Psammolestes Tertius Lent & Ravazi et al. Parasites Vectors (2021) 14:350 https://doi.org/10.1186/s13071-021-04854-8 Parasites & Vectors RESEARCH Open Access Trends in evolution of the Rhodniini tribe (Hemiptera, Triatominae): experimental crosses between Psammolestes tertius Lent & Jurberg, 1965 and P. coreodes Bergroth, 1911 and analysis of the reproductive isolating mechanisms Amanda Ravazi1†, Jader de Oliveira2,3†, Fabricio Ferreria Campos4, Fernanda Fernandez Madeira4, Yago Visinho dos Reis1, Ana Beatriz Bortolozo de Oliveira4, Maria Tercília Vilela de Azeredo‑Oliveira4, João Aristeu da Rosa3, Cleber Galvão5* and Kaio Cesar Chaboli Alevi1,2,3 Abstract Background: The tribe Rhodniini is a monophyletic group composed of 24 species grouped into two genera: Rhod- nius and Psammolestes. The genus Psammolestes includes only three species, namely P. coreodes, P. tertius and P. arthuri. Natural hybridization events have been reported for the Rhodniini tribe (for genus Rhodnius specifcally). Information obtained from hybridization studies can improve our understanding of the taxonomy and systematics of species. Here we report the results from experimental crosses performed between P. tertius and P. coreodes and from subsequent analyses of the reproductive and morphological aspects of the hybrids. Methods: Crossing experiments were conducted between P. tertius and P. coreodes to evaluate the pre‑ and post‑ zygotic barriers between species of the Rhodniini tribe. We also performed cytogenetic analyses of the F1 hybrids, with a focus on the degree of pairing between the homeologous chromosomes, and morphology studies of the male gonads to evaluate the presence of gonadal dysgenesis. Lastly, we analyzed the segregation of phenotypic characteristics. Results: Interspecifc experimental crosses demonstrated intrageneric genomic compatibility since hybrids were produced in both directions. However, these hybrids showed a high mortality rate, suggesting a post‑zygotic barrier resulting in hybrid unviability. The F1 hybrids that reached adulthood presented the dominant phenotypic segrega‑ tion pattern for P. tertius in both directions. These insects were then intercrossed; the hybrids were used in the cross between P. tertius ♀ P. coreodes ♂ died before oviposition, and the F1 hybrids of P. coreodes ♀ x P. tertius ♂ oviposited and their F2 hybrids ×hatched (however, all specimens died after hatching, still in frst‑generation nymph stage, point‑ ing to a hybrid collapse event). Morphological analyses of male gonads from F1 hybrids showed that they did not *Correspondence: [email protected] †Amanda Ravazi and Jader de Oliveira are co‑frst authors 5 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, RJ 21040‑360, Brazil Full list of author information is available at the end of the article © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Ravazi et al. Parasites Vectors (2021) 14:350 Page 2 of 8 have gonadal dysgenesis. Cytogenetic analyses of these triatomines showed that there were metaphases with 100% pairing between homeologous chromosomes and metaphases with pairing errors. Conclusion: The results of this study demonstrate that Psammolestes spp. have intrageneric genomic compat‑ ibility and that post‑zygotic barriers, namely unviability of hybrid and hybrid collapse, resulted in the breakdown of the hybrids of P. tertius and P. coreodes, confrming the specifc status of species based on the biological concept of species. Keywords: Triatomines, Hybridization, Psammolestes genus, Hybrid’s unviability, Hybrid collapse Background and Venezuela [12, 13]. Phylogenetic and cytogenetic Chagas disease is a neglected disease which afects analyses suggest that this genus is monophyletic [14, 15]. about 8 million people worldwide, with approximately Monteiro et al. [14] suggested that perhaps Psammolestes 25 million people at risk of infection. Treatment with should be regarded as a specialized lineage of Rhodnius the anti-trypanosomatids benznidazole and nifurtimox from the prolixus group because the genus Psammo- is more efective in the acute phase of the disease than lestes and species of the prolixus group share a com- in the chronic phase [1, 2]. Chagas disease is caused by mon ancestral form, which highlights the paraphyly of the protozoan Trypanosoma cruzi (Chagas, 1909) (Kine- the genus Rhodnius. Soares et al. [9] also suggested that toplastida, Trypanosomatidae) and the main form of Psammolestes is derived from an ancestral form similar transmission is through hematophagous insects known to R. robustus Larrousse, 1927, and de Paula et al. [16] as triatomines [2]. Currently, 156 species of triatomines, suggested that the species P. coreodes and P. tertius origi- divided into 18 genera and fve tribes [3–5], have been nated by vicariance. identifed, and all are considered to be potential Chagas de Paula et al. [16] also suggested that hydrological disease vectors. connections between the Araguaia–Amazon basins in Te tribe Rhodniini Pinto, 1926 is a monophyletic the Early and Middle Miocene [20.4–9.0 million years group composed of 24 species [3, 5–7] grouped into two ago (Mya)] would be a possible event that split the cis- genera that are morphologically and ecologically distinct: Andean + trans-Andean clades of the R. domesticus the members genus genus Rhodnius Stål, 1859 have long Neiva & Pinto, 1923 + Psammolestes + prolixus group thin legs and a long head, and live mainly in palm trees, (15.2 Mya). Tese authors indicated that this connec- while members of genus Psammolestes Bergroth, 1911 tion would incorporate the Pantanal system in the Upper have a short head, strong legs, wide femora, a very wide Miocene–Lower Miocene (10.0–4.5 Mya), resulting in rostrum (the widest in the subfamily) and live in nests of the separation of the Pantanal system from the Atlan- birds of the family Furnariidae [8]. Te inclusion of these tic Forest system, an event that may have contributed to two genera within the Rhodniini tribe is based on their the formation of Psammolestes species at a time when mainly arboreal behavior and the presence of post-ocular P. coreodes and P. tertius originated (4.98 Mya). On the tuberosities [7]. other hand, Soares et al. [9] suggested that Psammo- Rhodnius is a paraphyletic genus formed by 21 species lestes spp. spread from the Amazon region northward divided into the trans-Andean Rhodnius clade (pallescens into the llanos of Venezuela (where P. arthuri is abundant group) and the cis-Andean Rhodnius clade (pictipes + in Furnariidae nests) and southeastward into the Caat- prolixus groups) [5–7, 9]. Te event of paraphilia is sup- inga–Cerrado path of Central Brazil (with subsequent ported by the greater evolutionary proximity of the spe- diferentiation of P. tertius along a north–south cline and cies of the prolixus group with the genus Psammolestes P. coreodes in the Chaco region of Argentina and Para- which groups these species into a single clade [6, 10]. guay) [14, 17]. Based on this phenomenon, Hypsa et al. [11] proposed Events of natural hybridization have been reported changing the name of the genus including Psammolestes for the Rhodniini tribe (for the genus Rhodnius spe- spp. to Rhodnius: P. arthuri (Pinto, 1926) for R. arthuri cifcally) [18]. Information gained from hybridization (Pinto, 1926), P. coreodes Bergroth, 1911 for R. coreodes studies can further our understanding of the taxonomy (Bergroth, 1911) and P. tertius Lent & Jurberg, 1965 for R. and systematics of species, and be used to analyze the tertius (Lent & Jurberg, 1965). isolating mechanisms that limit gene fow between Te distribution of species included in genus Psam- species, and experimental crosses can be employed to molestes is restricted to Latin America, with P. coreodes establish the role of natural hybridization in generating being reported in Argentina, Bolivia, Brazil and Paraguay, new genetic variants (that may lead to adaptive evolu- P. tertius in Brazil and Peru and P. arthuri in Colombia tion and/or in founding new evolutionary lineages) [19, Ravazi et al. Parasites Vectors (2021) 14:350 Page 3 of 8 20]. In this context, we performed, for the frst time, Cytogenetic analysis experimental crosses between P. tertius and P. core- After the experimental crosses, the F1 males were odes and analyzed the reproductive and morphological dissected and the testes removed and stored in a aspects of the hybrids in order to
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