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The puzzling mitochondrial phylogeography of the black soldier fly (Hermetia illucens), the commercially most important insect protein species

BACKGROUND: The black soldier fly (Diptera: Stratiomyidae, Hermetia illucens) is renowned for its bioconversion ability of organic matter, and is the worldwide most widely used source of insect protein. Despite varying extensively in morphology, it is widely assumed that all black soldier flies belo...

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Autores principales: Ståhls, Gunilla, Meier, Rudolf, Sandrock, Christoph, Hauser, Martin, Šašić Zorić, Ljiljana, Laiho, Elina, Aracil, Andrea, Doderović, Jovana, Badenhorst, Rozane, Unadirekkul, Phira, Mohd Adom, Nur Arina Binte, Wein, Leo, Richards, Cameron, Tomberlin, Jeffery K., Rojo, Santos, Veselić, Sanja, Parviainen, Tuure
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7247124/
https://www.ncbi.nlm.nih.gov/pubmed/32448128
http://dx.doi.org/10.1186/s12862-020-01627-2
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author Ståhls, Gunilla
Meier, Rudolf
Sandrock, Christoph
Hauser, Martin
Šašić Zorić, Ljiljana
Laiho, Elina
Aracil, Andrea
Doderović, Jovana
Badenhorst, Rozane
Unadirekkul, Phira
Mohd Adom, Nur Arina Binte
Wein, Leo
Richards, Cameron
Tomberlin, Jeffery K.
Rojo, Santos
Veselić, Sanja
Parviainen, Tuure
author_facet Ståhls, Gunilla
Meier, Rudolf
Sandrock, Christoph
Hauser, Martin
Šašić Zorić, Ljiljana
Laiho, Elina
Aracil, Andrea
Doderović, Jovana
Badenhorst, Rozane
Unadirekkul, Phira
Mohd Adom, Nur Arina Binte
Wein, Leo
Richards, Cameron
Tomberlin, Jeffery K.
Rojo, Santos
Veselić, Sanja
Parviainen, Tuure
author_sort Ståhls, Gunilla
collection PubMed
description BACKGROUND: The black soldier fly (Diptera: Stratiomyidae, Hermetia illucens) is renowned for its bioconversion ability of organic matter, and is the worldwide most widely used source of insect protein. Despite varying extensively in morphology, it is widely assumed that all black soldier flies belong to the same species, Hermetia illucens. We here screened about 600 field-collected and cultured flies from 39 countries and six biogeographic regions to test this assumption based on data for three genes (mitochondrial COI, nuclear ITS2 & 28S rDNA) and in order to gain insights into the phylogeography of the species. RESULTS: Our study reveals a surprisingly high level of intraspecific genetic diversity for the mitochondrial barcoding gene COI (divergences up to 4.9%). This level of variability is often associated with the presence of multiple species, but tested nuclear markers (ITS2 and 28S rDNA) were invariant and fly strain hybridization experiments under laboratory conditions revealed reproductive compatibility. COI haplotype diversity is not only very high in all biogeographic regions (56 distinct haplotypes in total), but also in breeding facilities and research centers from six continents (10 haplotypes: divergences up to 4.3%). The high genetic diversity in fly-breeding facilities is mostly likely due to many independent acquisitions of cultures via sharing and/or establishing new colonies from field-collected flies. However, explaining some of the observed diversity in several biogeographic regions is difficult given that the origin of the species is considered to be New World (32 distinct haplotypes) and one would expect severely reduced genetic diversity in the putatively non-native populations in the remaining biogeographic regions. However, distinct, private haplotypes are known from the Australasian (N = 1), Oriental (N = 4), and the Eastern Palearctic (N = 4) populations. We reviewed museum specimen records and conclude that the evidence for introductions is strong for the Western Palearctic and Afrotropical regions which lack distinct, private haplotypes. CONCLUSIONS: Based on the results of this paper, we urge the black soldier fly community to apply molecular characterization (genotyping) of the fly strains used in artificial fly-breeding and share these data in research publications as well as when sharing cultures. In addition, fast-evolving nuclear markers should be used to reconstruct the recent invasion history of the species.
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spelling pubmed-72471242020-06-01 The puzzling mitochondrial phylogeography of the black soldier fly (Hermetia illucens), the commercially most important insect protein species Ståhls, Gunilla Meier, Rudolf Sandrock, Christoph Hauser, Martin Šašić Zorić, Ljiljana Laiho, Elina Aracil, Andrea Doderović, Jovana Badenhorst, Rozane Unadirekkul, Phira Mohd Adom, Nur Arina Binte Wein, Leo Richards, Cameron Tomberlin, Jeffery K. Rojo, Santos Veselić, Sanja Parviainen, Tuure BMC Evol Biol Research Article BACKGROUND: The black soldier fly (Diptera: Stratiomyidae, Hermetia illucens) is renowned for its bioconversion ability of organic matter, and is the worldwide most widely used source of insect protein. Despite varying extensively in morphology, it is widely assumed that all black soldier flies belong to the same species, Hermetia illucens. We here screened about 600 field-collected and cultured flies from 39 countries and six biogeographic regions to test this assumption based on data for three genes (mitochondrial COI, nuclear ITS2 & 28S rDNA) and in order to gain insights into the phylogeography of the species. RESULTS: Our study reveals a surprisingly high level of intraspecific genetic diversity for the mitochondrial barcoding gene COI (divergences up to 4.9%). This level of variability is often associated with the presence of multiple species, but tested nuclear markers (ITS2 and 28S rDNA) were invariant and fly strain hybridization experiments under laboratory conditions revealed reproductive compatibility. COI haplotype diversity is not only very high in all biogeographic regions (56 distinct haplotypes in total), but also in breeding facilities and research centers from six continents (10 haplotypes: divergences up to 4.3%). The high genetic diversity in fly-breeding facilities is mostly likely due to many independent acquisitions of cultures via sharing and/or establishing new colonies from field-collected flies. However, explaining some of the observed diversity in several biogeographic regions is difficult given that the origin of the species is considered to be New World (32 distinct haplotypes) and one would expect severely reduced genetic diversity in the putatively non-native populations in the remaining biogeographic regions. However, distinct, private haplotypes are known from the Australasian (N = 1), Oriental (N = 4), and the Eastern Palearctic (N = 4) populations. We reviewed museum specimen records and conclude that the evidence for introductions is strong for the Western Palearctic and Afrotropical regions which lack distinct, private haplotypes. CONCLUSIONS: Based on the results of this paper, we urge the black soldier fly community to apply molecular characterization (genotyping) of the fly strains used in artificial fly-breeding and share these data in research publications as well as when sharing cultures. In addition, fast-evolving nuclear markers should be used to reconstruct the recent invasion history of the species. BioMed Central 2020-05-24 /pmc/articles/PMC7247124/ /pubmed/32448128 http://dx.doi.org/10.1186/s12862-020-01627-2 Text en © The Author(s) 2020 Open AccessThis 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://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Ståhls, Gunilla
Meier, Rudolf
Sandrock, Christoph
Hauser, Martin
Šašić Zorić, Ljiljana
Laiho, Elina
Aracil, Andrea
Doderović, Jovana
Badenhorst, Rozane
Unadirekkul, Phira
Mohd Adom, Nur Arina Binte
Wein, Leo
Richards, Cameron
Tomberlin, Jeffery K.
Rojo, Santos
Veselić, Sanja
Parviainen, Tuure
The puzzling mitochondrial phylogeography of the black soldier fly (Hermetia illucens), the commercially most important insect protein species
title The puzzling mitochondrial phylogeography of the black soldier fly (Hermetia illucens), the commercially most important insect protein species
title_full The puzzling mitochondrial phylogeography of the black soldier fly (Hermetia illucens), the commercially most important insect protein species
title_fullStr The puzzling mitochondrial phylogeography of the black soldier fly (Hermetia illucens), the commercially most important insect protein species
title_full_unstemmed The puzzling mitochondrial phylogeography of the black soldier fly (Hermetia illucens), the commercially most important insect protein species
title_short The puzzling mitochondrial phylogeography of the black soldier fly (Hermetia illucens), the commercially most important insect protein species
title_sort puzzling mitochondrial phylogeography of the black soldier fly (hermetia illucens), the commercially most important insect protein species
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7247124/
https://www.ncbi.nlm.nih.gov/pubmed/32448128
http://dx.doi.org/10.1186/s12862-020-01627-2
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