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Molecular Clock and Phylogeny of Anopheles Species of the Subgenus Nyssorhynchus

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bioRxiv preprint doi: https://doi.org/10.1101/262147; this version posted February 8, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Molecular Clock and Phylogeny of Anopheles species of the subgenus Nyssorhynchus 2 (Diptera: Culicidae). 3 4 Richard Hoyos-López 5 6 Grupo de Investigación en Resistencia Bacteriana y Enfermedades Tropicales, Facultad de 7 Ciencias de la Salud. Universidad del Sinú, Montería, Córdoba, Colombia. 8 9 Author for correspondence: Richard Hoyos López, Tel: 057+430 9394, E-mail: 10 [email protected]. 11 12 13 14 15 16 17 18 19 bioRxiv preprint doi: https://doi.org/10.1101/262147; this version posted February 8, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 20 Abstract 21 The main Phylogenetic hypothesis supporting the Myzorhynchella section as a natural 22 group, but the sections Albimanus and Argyritarsis, do not present clearly resolved 23 relationships, nor is it possible to recover the monophyly of both sections, even within 24 these sections of Nyssorhynchus; it has not been possible identify the relationships between 25 the species that make up these taxonomic subdivisions (Sallum, 2000, Sallum, 2002, 26 Bourke, 2011, Foster, 2013). This lack of resolution has been attributed to the effect of few 27 species for phylogenetic studies, making difficult the determination of monophyly of many 28 groups, subgroups and complexes within sections Albimanus and Argyritarsis 29 We infer the phylogeny of the subgenus Nyssorhynchus through the sequences 30 characterized for the molecular markers ND6, COI-Barcode, White and CAD, in addition 31 we calculate the times of divergence for the main lineages corresponding to the sections 32 Albimanus, Argyritarsis and Myzorhynchella using Bayesian approaches. 33 34 Key words: Anopheles, Nyssorhynchus, Phylogeny, Molecular Clock. 35 36 37 38 39 40 bioRxiv preprint doi: https://doi.org/10.1101/262147; this version posted February 8, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 41 1. Introduction 42 Malaria is among the most important diseases worldwide with approximately 216 million 43 cases registered for 2011 and an estimated 655,000 deaths in 2010 (Sachs, 2002, WHO, 44 2011). This disease constitutes an important obstacle for the economic and social 45 development of the affected countries, despite the control programs that have helped to 46 reduce its incidence since 2000, it has been observed that the maintenance of effectiveness 47 in the control programs has decayed and consequently allowed historical re-emergence in 48 endemic regions and rural areas of South-America (Cohen, 2012). 49 The identification of species is essential for vector incrimination, the measurement of 50 epidemiological risk and the development of management programs for malaria (Sinka, 51 2010); the focus of these works are guided to mosquitoes belonging to the genus 52 Anopheles, which contains all known malaria vectors, with a significant number of 53 representatives considered complex species (Foster, 2013), these are considered 54 morphologically indistinguishable and in other cases phenotypic plasticity makes 55 identification difficult, due to similarity with closely related species (Sallum, 2000). In 56 these cases of taxonomic complexity, only approaches with markers and molecular tools 57 allow to resolve the identity, relationships between species and vector incrimination (Porter 58 & Collins, 1991, Paskewitz, 1993, Cornel, 1996, Cywinska, 2006, Marelli, 2006, Zapata, 59 2007, Hoyos-López et al. 2012a, Hoyos-López et al. 2012b, Hoyos et al. 2015a, Hoyos et 60 al. 2015b, Hoyos et al. 2015c, Hoyos et al. 2016, Hoyos et al. 2017). 61 Mosquitoes of the subfamily Anophelinae include 465 formally recognized and 50 62 undescribed species belonging to species complexes (Harbach, 2007, Foster, 2013), all of 63 them divided into three genera: Anopheles, Bironella and Chagasia. bioRxiv preprint doi: https://doi.org/10.1101/262147; this version posted February 8, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 64 Anopheles is subdivided into seven subgenres: Anopheles, Baimaia, Cellia, Kerteszia, 65 Lophopodomyia, Nyssorhynchus and Stethomyia. Nine species of the genus Anopheles are 66 considered primary vectors in America, three species belong to the subgenus Anopheles and 67 six to Nyssorhynchus (Sinka, 2010), however, the latter encompasses at least twelve species 68 considered secondary vectors because of their local and / or regional importance ( Bourke, 69 2011). The identification and separation of anophelines has involved research in 70 phylogenetics and phylogeography, mainly in species of recognized epidemiological 71 importance (Porter & Collins, 1991, Paskewitz, 1993, Cornel, 1996, Sallum, 2000, 72 Cywinska, 2006, Marelli, 2006, Zapata, 2007; Bourke, 2011; Foster, 2013). 73 The subgenus Nyssorhynchus presents a neotropical distribution, including 39 formally 74 recognized species and around six not described but differentiable by molecular markers, 75 subdivided into three sections: Albimanus, Argyritarsis and Myzorhynchella. Sallum et al. 76 (2000) using morphological characters and a wide range of species, is able to determine the 77 monophyly of the subfamily Anophelinae and the subgenus Cellia, Kerteszia and 78 Nyssorhynchus, which was subsequently corroborated with evidence from nuclear and 79 mitochondrial gene sequences (Krzywinsky 2011; Sallum 2002; Harbach 2007), however, 80 the phylogenetic relationships within the subgenus Nyssorhynchus were not clarified. 81 Bourke et al. (2010) and Foster et al. (2013), using DNA sequences from the ND6, White, 82 COI and CAD markers, respectively, provides evidence of statistical support for some 83 lineages, but clear genealogical discrepancies of inferred Bayesian trees are observed for 84 each marker. 85 The concatenated Bayesian topologies allow to support the Myzorhynchella section as a 86 natural group, but the sections Albimanus and Argyritarsis, do not present clearly resolved bioRxiv preprint doi: https://doi.org/10.1101/262147; this version posted February 8, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 87 relationships, nor is it possible to recover the monophyly of both sections, even within 88 these sections of Nyssorhynchus; it has not been possible identify the relationships between 89 the species that make up these taxonomic subdivisions (Sallum, 2000, Sallum, 2002, 90 Bourke, 2011, Foster, 2013). This lack of resolution has been attributed to the effect of few 91 species for phylogenetic studies, making difficult the determination of monophyly of many 92 groups, subgroups and complexes within sections Albimanus and Argyritarsis, also to the 93 effect of low phylogenetic signal for ND6 genes + White used by Bourke et al. (2010) and 94 CAD + COI-Barcode by Foster et al. (2013). Reidenbach et al. (2009), estimates the first 95 approach to the time of divergence between two species of the genus Anopheles, belonging 96 to the subgenera Stethomyia (Anopheles gambiae) and Cellia (Anopheles atroparvus), 97 inferring a separation of these taxa about 20-24 million years ago. 98 Currently, it is considered that a large number of sequences from nuclear and mitochondrial 99 genes can solve phylogenetic problems and infer divergence times like the study by Regier 100 & Zwick (2008), who used sequences of 62 nuclear genes coding for proteins and were able 101 to infer the phylogeny of the phylum Arthropoda and the work of Reidenbach (2009), 102 characterizing seven molecular markers to infer the phylogeny of the subfamilies, tribes 103 and genera representative of the Culicidae family. 104 In this research, we infer the phylogeny of the subgenus Nyssorhynchus through the 105 sequences characterized for the molecular markers ND6, COI-Barcode, White and CAD, in 106 addition we calculate the times of divergence for the main lineages corresponding to the 107 sections Albimanus, Argyritarsis and Myzorhynchella using Bayesian approaches. 108 bioRxiv preprint doi: https://doi.org/10.1101/262147; this version posted February 8, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 109 Material and Methods 110 Preparation of sequences and alignments. 111 Through Genbank it was possible to obtain the sequences belonging to the ND6 and White 112 markers described by Bourke (2011), and those used by Foster (2013): CAD and COI- 113 Barcode. Manually aligning sets of 40 sequences for each marker in 22 species of the 114 subgenus Nyssorhynchus and two external groups (Anopheles, Stethomyia) (Table 1). 115 Species with little representation were eliminated and emphasis was placed on those that 116 presented information for all the genes used. In this way, individual and one concatenated 117 alignments were constructed (Table 1). For the White and CAD nuclear genes, only blocks 118 with clear positional homology were used, discarding gaps and blocks with multiple 119 ambiguous sites. In COI-Barcode and ND6, amino acid translation was performed to avoid 120 nuclear sequences of mitochondrial origin (NUMTs), pseudogenes and unedited sequences 121 of Genbank.
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  • Identification Key to the Anopheles Mosquitoes of South America (Diptera: Culicidae). III. Male Genitalia

    Identification Key to the Anopheles Mosquitoes of South America (Diptera: Culicidae). III. Male Genitalia

    Sallum et al. Parasites Vectors (2020) 13:542 https://doi.org/10.1186/s13071-020-04300-1 Parasites & Vectors RESEARCH Open Access Identifcation key to the Anopheles mosquitoes of South America (Diptera: Culicidae). III. Male genitalia Maria Anice Mureb Sallum1*, Ranulfo González Obando2, Nancy Carrejo2 and Richard C. Wilkerson3,4,5 Abstract Background: Accurate identifcation of the species of Anopheles Meigen, 1818 requires careful examination of all life stages. However, morphological characters, especially those of the females and fourth-instar larvae, show some degree of polymorphism and overlap among members of species complexes, and sometimes even within progenies. Characters of the male genitalia are structural and allow accurate identifcation of the majority of species, excluding only those in the Albitarsis Complex. In this key, based on the morphology of the male genitalia, traditionally used important characters are exploited together with additional characters that allow robust identifcation of male Anoph- eles mosquitoes in South America. Methods: Morphological characters of the male genitalia of South American species of the genus Anopheles were examined and employed to construct a comprehensive, illustrated identifcation key. For those species for which specimens were not available, illustrations were based on published illustrations. Photographs of key characters of the genitalia were obtained using a digital Canon Eos T3i attached to a light Diaplan Leitz microscope. The program Helicon Focus was used to build single in-focus images by stacking multiple images of the same structure. Results: An illustrated key to South American species of Anopheles based on the morphology of the male genitalia is presented, together with a glossary of morphological terms.