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Drivers of Molecular and Morphometric Variation in Triatoma

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Drivers of Molecular and Morphometric Variation in Triatoma Kamimura et al. Parasites Vectors (2020) 13:455 https://doi.org/10.1186/s13071-020-04340-7 Parasites & Vectors RESEARCH Open Access Drivers of molecular and morphometric variation in Triatoma brasiliensis (Hemiptera: Triatominae): the resolution of geometric morphometrics for populational structuring on a microgeographical scale Edgard H. Kamimura1†, Maria Carolina Viana1†, Maurício Lilioso1, Fernanda H. M. Fontes1, Dayane Pires‑Silva1, Carolina Valença‑Barbosa1, Ana L. Carbajal‑de‑la‑Fuente2,3, Elaine Folly‑Ramos4, Vera N. Solferin1, Patricia J. Thyssen1, Jane Costa5† and Carlos E. Almeida1*† Abstract Background: The protozoan Trypanosoma cruzi circulates in semiarid areas of northeastern Brazil in distinct ecotopes (sylvatic, peridomestic and domestic) where Triatoma brasiliensis Neiva, 1911 is the most important Chagas disease vector. In this study, we analyzed microevolutionary and demographic aspects of T. brasiliensis populations at the ecotypic, micro and macro‑geographic scales by combining morphometrics and molecular results. Additionally, we aimed to address the resolution of both markers for delimiting populations in distinct scales. Methods: We sampled populations of T. brasiliensis from distinct ecotypic and geographic sites in the states Rio Grande do Norte (RN) and Paraíba (PB). The geometric morphometry was carried out with 13 landmarks on the right wings (n 698) and the genetic structure was assessed by sequencing a region of cytochrome b mitochondrial gene (n 221). = = Mahalanobis distance (MD) and coefcient of molecular diferentiation (ΦST) were calculated among all pairs of popula‑ tions. The results of comparisons generated MD and ΦST dendrograms, and graphics of canonical variate analysis (CVA). Results: Little structure was observed for both markers for macro‑geographic scales. Mantel tests comparing geo‑ graphic, morphometric and genetic matrices showed low correlation (all R2 < 0.35). The factorial graphics built with the CVA evidenced population delimitation for the morphometric data at micro‑geographic scales. Conclusions: We believe that T. brasiliensis carries in its genotype a source of information to allow the phenotypical plasticity across its whole distribution for shaping populations, which may have caused a lack of population delimi‑ tation for CVAs in morphometric analysis for macro‑geographic scale analysis. On the other hand, the pattern of morphometric results in micro‑geographic scales showed well‑defned groups, highlighting the potential of this tool to inferences on the source for infestation. Keywords: Triatomine ecology, Population structure, Phenotypic plasticity, Chagas disease, Vectors *Correspondence: [email protected]; [email protected] †Edgard H. Kamimura, Maria Carolina Viana, Jane Costa and Carlos E. Almeida Joint frst and senior authors 1 Instituto de Biologia, Universidade Estadual de Campinas (UNICAMP), Campinas, Brazil Full list of author information is available at the end of the article © The Author(s) 2020. 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. Kamimura et al. Parasites Vectors (2020) 13:455 Page 2 of 15 Background forms was considered subspecies (T. b. macromelasoma), Chagas disease is among the most important neglected also because little genetic distance was observed with T. diseases in Latin American countries. Te transmission b. brasiliensis [17]. Later, T. sherlocki was included in this classically occurs via vector insects of the subfamily Tri- species complex by using the information on the varia- atominae (Hemiptera: Heteroptera: Reduviidae). Tese tion in cytochrome b (cytb) and 16S mitochondrial genes insect vectors may transmit the disease when they are [18], which was confrmed through cytogenetic analyzes infected with the parasite Trypanosoma cruzi (Chagas, and experimental crosses [19, 20]. Other species were 1909) (Kinetoplastida: Trypanosomatidae), the etiologi- included in this group or revalidated, such as T. lenti and cal agent of the illness. Although the disease’s incidence T. bahiensis [21]. Finally, T. petrocchiae was also consid- has declined in recent decades due to intense programs to ered a member of this monophyletic group, in a study combat the main domiciliated vectors, it is estimated that combining geometric morphometrics and information six to eight million people are still infected worldwide [1]. on multiple mitochondrial genes (12S + 16S + cox1 + More than 65 species of triatomines have been recorded cytb) [22]. Te non-monophyly of the Brasiliensis sub- in Brazil, but few exhibit synanthropic behaviors, such as complex also proposed the exclusion of T. melanocephala Triatoma infestans, Panstrongylus megistus (Burmeister, and T. vitticeps [22], which was then confrmed through 1835), T. brasiliensis Neiva, 1911, T. pseudomaculata Cor- cytogenetic analyzes [23, 24]. Recently, a key was released rêa & Espínola, 1964 and T. sordida (Stål, 1859) [2]. Te to identify each member of this species complex [7]. For Brazilian Northeast, one of the poorest and underdevel- simplicity, we hereafter refer to the taxon used in this oped regions of the country, raises concern in the context study (T. b. brasiliensis) as T. brasiliensis. of Chagas disease transmission because it is an area of For the T. brasiliensis species complex, molecu- infestation by T. brasiliensis and T. pseudomaculata, native lar studies have been mainly based on the variation of triatomines of difcult control and widespread in the sem- mitochondrial DNA genes [5, 17, 25] and, geometric iarid Northeast. Whereas T. pseudomaculata is more asso- morphometrics has already been applied for the species ciated with birds [3] (refractory to T. cruzi infection), T. [26]. Molecular and morphometric markers have been brasiliensis is associated with mammals, which are poten- combined [22, 27], but not under the focus of gamma tial parasite reservoirs [4, 5]. Additionally, T. brasiliensis systematics (intra-specifcally). In this study, we analyzed is the most frequently Chagas disease vector collected in microevolutionary and demographic aspects of T. bra- human domiciles and is considered the most important siliensis populations at the ecotypic, micro and macro- triatomine species in the region [6]. geographical scales by combining morphometrics and Te current status of the T. brasiliensis species com- molecular approaches. plex is based on a group of monophyletic taxa that occur in rocky outcrops of the semiarid region of the Brazil- Methods ian Northeast, including seven species: T. brasiliensis; T. Insects bahiensis Sherlock & Serafm, 1967; T. juazeirensis Costa Triatomine captures were conducted in the State of Rio & Felix, 2007; T. lenti Sherlock & Serafm, 1967; T. melan- Grande do Norte (RN), in the municipalities of Caicó, ica (Neiva & Lent, 1941); T. petrocchiae Pinto & Barreto, Currais Novos and Marcelino Vieira, whereas in the State 1925; and T. sherlocki Papa, Jurberg, Carcavallo, Cerque- of Paraíba (PB), insects were collected in the municipali- ira & Barata, 2002; in which T. brasiliensis is divided into ties of Condado, Cajazeiras, Santa Teresinha, São José two subspecies: T. b. brasiliensis Neiva, 1911 and T. b. de Espinharas, São Mamede and Emas (Fig. 1). Te sam- macromelasoma Galvão, 1956 [7]. Lent & Wygodzinsky pling covered a range of 240 km (East-West) and 95 km ′ ″ ′ ″ [8] observed that across its distribution, T. brasiliensis (North-South) (− 6°58 48.0 to − 6°08 49.2 latitude and ′ ″ ′ ″ (s.l.) exhibited numerous chromatic forms and empha- − 38°35 27.6 to − 36°29 09.6 longitude). Te sampled sized it should be better investigated. Tis led Costa and spots were within the biogeographical zone known as colleagues to conduct a set of investigations based on Caatinga, a mosaic of xerophytic, deciduous, semiarid biology, ecology, phylogeny, experimental crossings [9– thorn scrub and forest [28]. All captures were conducted 13] among others. Te Brasiliensis subcomplex was pro- manually with the aid of tweezers. We defned three dis- posed by Schofeld & Galvão [14] based on the ecological tinct ecotopes: (i) the sylvatic ecotopes (primary) were data, geographical distribution and morphology, which represented by rocky outcrops; (ii) the domestic ecotopes included T. melanocephala Neiva & Pinto, 1923 and T. were considered as the indoor spaces where humans vitticeps (Stal, 1859) (as uncertain). Te chromatic varia- sleep or work; and (iii) the peridomestic ecotopes were tion combined with genetic information resulted in rais- defned as the spaces surrounding domiciles,
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