Genetic diversity and phylogenetic relationships of coevolving symbiont-harboring insect trypanosomatids, and their neotropical dispersal by invader African blowflies (Calliphoridae)

This study is about the inter- and intra-specific genetic diversity of trypanosomatids of the genus Angomonas, and their association with Calliphoridae (blowflies) in Neotropical and Afrotropical regions. Microscopic examination of 3,900 flies of various families, mostly Calliphoridae, revealed that 31% of them harbored trypanosomatids. Small subunit rRNA (SSU rRNA) barcoding showed that Angomonas predominated (46%) over the other common trypanosomatids of blowflies of genera Herpetomonas and Wallacemonas. Among Angomonas spp., A. deanei was much more common than the two-other species, A. desouzai and A. ambiguus. Phylogenetic analyses based on SSU rRNA, glycosomal glyceraldehyde-3-phosphate dehydrogenase (gGAPDH) and internal transcribed spacer rDNA (ITS rDNA) sequences revealed a marked genetic diversity within A. deanei, which comprised four infraspecific genotypes (Dea1– Dea4), and four corresponding symbiont genotypes (Kcr1–Kcr4). Host and symbiont phylogenies were highly congruent corroborating their co-divergence, consistent with host-symbiont interdependent metabolism and symbiont reduced genomes shaped by a long coevolutionary history. We compared the diversity of Angomonas/symbionts from three genera of blowflies, Lucilia, Chrysomya and Cochliomyia. A. deanei, A. desouzai, and A. ambiguus were found in the three genera of blowflies in South America. In Africa, A. deanei and A. ambiguus were identified in Chrysomya. The absence of A. desouzai in Africa and its presence in Neotropical Cochliomyia and Lucilia suggests parasite spillback of A. desouzai into Chrysomya, which was most likely introduced four decades ago from Africa into the Neotropic. The absence of correlation between parasite diversity and geographic and genetic distances, with identical genotypes of A. deanei found in the Neotropic and Afrotropic, is consistent with disjunct distribution due to the recent human-mediated transoceanic dispersal of Angomonas by Chrysomya. This study provides the most comprehensive data gathered so far on the genetic repertoires of a genus of trypanosomatids found in flies from a wide geographical range.The PROAFRICA, INCT-EPIAMO, and PROSUL programs of CNPq, PNIPB of Capes, and FAPESP (Process 2016/07487-0). CAPEs (PNPD) granted a postdoctoral scholarship to TB.http://www.frontiersin.org/Microbiologyam2018Veterinary Tropical Disease

FIGURE 7 in Lecithoceridae (Lepidoptera) of Madagascar: I. Descriptions of eighteen new species of Torodora Meyrick, 1894

FIGURE 7. Torodora sogai Park & Koo, sp. nov.: A, adult, male (holotype); B, head with labial palpus, lateral view (paratype); C, under surface of wings (holotype); D, hind tibia (paratype); E, male genitalia (slide no. CIS-7369); F, ditto, aedeagus; G, uncus+gnathos (slide no. CIS-7368); H, abdominal segments VI–VIII.Published as part of Park, Kyu-Tek, Koo, Jun-Mo, Minet, Joël & Razafindranaivo, Victor, 2023, Lecithoceridae (Lepidoptera) of Madagascar: I. Descriptions of eighteen new species of Torodora Meyrick, 1894, pp. 151-184 in Zootaxa 5264 (2) on page 162, DOI: 10.11646/zootaxa.5264.2.1, http://zenodo.org/record/783631

FIGURE 4 in Lecithoceridae (Lepidoptera) of Madagascar: I. Descriptions of eighteen new species of Torodora Meyrick, 1894

FIGURE 4. Torodora larseni Park & Koo, sp. nov.: A, adult, male (holotype); B, head with labial palpus, lateral view; C, head, dorsal view; D, male genitalia (slide no. CIS-7478); E, ditto, aedeagus; F, abdomen.Published as part of Park, Kyu-Tek, Koo, Jun-Mo, Minet, Joël & Razafindranaivo, Victor, 2023, Lecithoceridae (Lepidoptera) of Madagascar: I. Descriptions of eighteen new species of Torodora Meyrick, 1894, pp. 151-184 in Zootaxa 5264 (2) on page 157, DOI: 10.11646/zootaxa.5264.2.1, http://zenodo.org/record/783631

FIGURE 5 in Lecithoceridae (Lepidoptera) of Madagascar: I. Descriptions of eighteen new species of Torodora Meyrick, 1894

FIGURE 5. Torodora toliarensis Park & Koo, sp. nov.: A, adult, male (holotype); B, head with labial palpus, lateral view; C, right wings; D, male genitalia (slide no. CIS-7373); E, ditto, aedeagus; F, abdomen.Published as part of <i>Park, Kyu-Tek, Koo, Jun-Mo, Minet, Joël & Razafindranaivo, Victor, 2023, Lecithoceridae (Lepidoptera) of Madagascar: I. Descriptions of eighteen new species of Torodora Meyrick, 1894, pp. 151-184 in Zootaxa 5264 (2)</i> on page 158, DOI: 10.11646/zootaxa.5264.2.1, <a href="http://zenodo.org/record/7836316">http://zenodo.org/record/7836316</a&gt

FIGURE 17 in Lecithoceridae (Lepidoptera) of Madagascar: I. Descriptions of eighteen new species of Torodora Meyrick, 1894

FIGURE 17. Torodora anosibensis Park & Minet, sp. nov.: A, adult, female (holotype); B, head with labial palpus, lateral view; C, female genitalia (slide no. CIS-7397).Published as part of <i>Park, Kyu-Tek, Koo, Jun-Mo, Minet, Joël & Razafindranaivo, Victor, 2023, Lecithoceridae (Lepidoptera) of Madagascar: I. Descriptions of eighteen new species of Torodora Meyrick, 1894, pp. 151-184 in Zootaxa 5264 (2)</i> on page 176, DOI: 10.11646/zootaxa.5264.2.1, <a href="http://zenodo.org/record/7836316">http://zenodo.org/record/7836316</a&gt

FIGURE 21 in Lecithoceridae (Lepidoptera) of Madagascar: I. Descriptions of eighteen new species of Torodora Meyrick, 1894

FIGURE 21. Torodora griveaudi Park & Minet, sp. nov.: A, adult, male (holotype); B, lateral view of adult; C, left wings; D, male genitalia (slide no. CIS-7364); E, ditto, aedeagus; F, posterior part (abdominal segments V–VII) of abdomen; G, abdominal sternum VIII.Published as part of Park, Kyu-Tek, Koo, Jun-Mo, Minet, Joël & Razafindranaivo, Victor, 2023, Lecithoceridae (Lepidoptera) of Madagascar: I. Descriptions of eighteen new species of Torodora Meyrick, 1894, pp. 151-184 in Zootaxa 5264 (2) on page 182, DOI: 10.11646/zootaxa.5264.2.1, http://zenodo.org/record/783631

FIGURE 18 in Lecithoceridae (Lepidoptera) of Madagascar: I. Descriptions of eighteen new species of Torodora Meyrick, 1894

FIGURE 18. Torodora convexula Park & Minet, sp. nov.: A, adult, female (holotype); B, head with labial palpus, lateral view; C, female genitalia (slide no. CIS-7371).Published as part of <i>Park, Kyu-Tek, Koo, Jun-Mo, Minet, Joël & Razafindranaivo, Victor, 2023, Lecithoceridae (Lepidoptera) of Madagascar: I. Descriptions of eighteen new species of Torodora Meyrick, 1894, pp. 151-184 in Zootaxa 5264 (2)</i> on page 178, DOI: 10.11646/zootaxa.5264.2.1, <a href="http://zenodo.org/record/7836316">http://zenodo.org/record/7836316</a&gt

FIGURE 19 in Lecithoceridae (Lepidoptera) of Madagascar: I. Descriptions of eighteen new species of Torodora Meyrick, 1894

FIGURE 19. Torodora sphenosa Park & Minet, sp. nov.: A, adult, female (holotype); B, right wings: C, antenna; D, head with labial palpus, lateral view; E, female genitalia (slide no. CIS-7360).Published as part of <i>Park, Kyu-Tek, Koo, Jun-Mo, Minet, Joël & Razafindranaivo, Victor, 2023, Lecithoceridae (Lepidoptera) of Madagascar: I. Descriptions of eighteen new species of Torodora Meyrick, 1894, pp. 151-184 in Zootaxa 5264 (2)</i> on page 179, DOI: 10.11646/zootaxa.5264.2.1, <a href="http://zenodo.org/record/7836316">http://zenodo.org/record/7836316</a&gt

FIGURE 12 in Lecithoceridae (Lepidoptera) of Madagascar: I. Descriptions of eighteen new species of Torodora Meyrick, 1894

FIGURE 12. Torodora zahamenensis Park & Koo, sp. nov.: A, adult, female (holotype); B, head with labial palpus, lateral view; C, female genitalia (slide no. CIS-7392).Published as part of Park, Kyu-Tek, Koo, Jun-Mo, Minet, Joël & Razafindranaivo, Victor, 2023, Lecithoceridae (Lepidoptera) of Madagascar: I. Descriptions of eighteen new species of Torodora Meyrick, 1894, pp. 151-184 in Zootaxa 5264 (2) on page 169, DOI: 10.11646/zootaxa.5264.2.1, http://zenodo.org/record/783631

FIGURE 11 in Lecithoceridae (Lepidoptera) of Madagascar: I. Descriptions of eighteen new species of Torodora Meyrick, 1894

FIGURE 11. Torodora septentriella Park & Koo, sp. nov.: A, adult, male (holotype); B, head with labial palpus, lateral view; C, male genitalia (slide no. CIS-7391); D, ditto, aedeagus; E, abdomen.Published as part of <i>Park, Kyu-Tek, Koo, Jun-Mo, Minet, Joël & Razafindranaivo, Victor, 2023, Lecithoceridae (Lepidoptera) of Madagascar: I. Descriptions of eighteen new species of Torodora Meyrick, 1894, pp. 151-184 in Zootaxa 5264 (2)</i> on page 167, DOI: 10.11646/zootaxa.5264.2.1, <a href="http://zenodo.org/record/7836316">http://zenodo.org/record/7836316</a&gt