Global population genetic structure and demographic trajectories of the black soldier fly, Hermetia illucens.

Allelic richness Approximate Bayesian computation Diptera Founder effect Genetic differentiation Genetic drift Invasive species Isolation by distance Serial introductions Stratiomyidae

Journal

BMC biology
ISSN: 1741-7007
Titre abrégé: BMC Biol
Pays: England
ID NLM: 101190720

Informations de publication

Date de publication:
05 05 2021
Historique:
received: 04 10 2020
accepted: 16 04 2021
entrez: 6 5 2021
pubmed: 7 5 2021
medline: 2 2 2022
Statut: epublish

Résumé

The black soldier fly (Hermetia illucens) is the most promising insect candidate for nutrient-recycling through bioconversion of organic waste into biomass, thereby improving sustainability of protein supplies for animal feed and facilitating transition to a circular economy. Contrary to conventional livestock, genetic resources of farmed insects remain poorly characterised. We present the first comprehensive population genetic characterisation of H. illucens. Based on 15 novel microsatellite markers, we genotyped and analysed 2862 individuals from 150 wild and captive populations originating from 57 countries on seven subcontinents. We identified 16 well-distinguished genetic clusters indicating substantial global population structure. The data revealed genetic hotspots in central South America and successive northwards range expansions within the indigenous ranges of the Americas. Colonisations and naturalisations of largely unique genetic profiles occurred on all non-native continents, either preceded by demographically independent founder events from various single sources or involving admixture scenarios. A decisive primarily admixed Polynesian bridgehead population serially colonised the entire Australasian region and its secondarily admixed descendants successively mediated invasions into Africa and Europe. Conversely, captive populations from several continents traced back to a single North American origin and exhibit considerably reduced genetic diversity, although some farmed strains carry distinct genetic signatures. We highlight genetic footprints characteristic of progressing domestication due to increasing socio-economic importance of H. illucens, and ongoing introgression between domesticated strains globally traded for large-scale farming and wild populations in some regions. We document the dynamic population genetic history of a cosmopolitan dipteran of South American origin shaped by striking geographic patterns. These reflect both ancient dispersal routes, and stochastic and heterogeneous anthropogenic introductions during the last century leading to pronounced diversification of worldwide structure of H. illucens. Upon the recent advent of its agronomic commercialisation, however, current human-mediated translocations of the black soldier fly largely involve genetically highly uniform domesticated strains, which meanwhile threaten the genetic integrity of differentiated unique local resources through introgression. Our in-depth reconstruction of the contemporary and historical demographic trajectories of H. illucens emphasises benchmarking potential for applied future research on this emerging model of the prospering insect-livestock sector.

Sections du résumé

BACKGROUND
The black soldier fly (Hermetia illucens) is the most promising insect candidate for nutrient-recycling through bioconversion of organic waste into biomass, thereby improving sustainability of protein supplies for animal feed and facilitating transition to a circular economy. Contrary to conventional livestock, genetic resources of farmed insects remain poorly characterised. We present the first comprehensive population genetic characterisation of H. illucens. Based on 15 novel microsatellite markers, we genotyped and analysed 2862 individuals from 150 wild and captive populations originating from 57 countries on seven subcontinents.
RESULTS
We identified 16 well-distinguished genetic clusters indicating substantial global population structure. The data revealed genetic hotspots in central South America and successive northwards range expansions within the indigenous ranges of the Americas. Colonisations and naturalisations of largely unique genetic profiles occurred on all non-native continents, either preceded by demographically independent founder events from various single sources or involving admixture scenarios. A decisive primarily admixed Polynesian bridgehead population serially colonised the entire Australasian region and its secondarily admixed descendants successively mediated invasions into Africa and Europe. Conversely, captive populations from several continents traced back to a single North American origin and exhibit considerably reduced genetic diversity, although some farmed strains carry distinct genetic signatures. We highlight genetic footprints characteristic of progressing domestication due to increasing socio-economic importance of H. illucens, and ongoing introgression between domesticated strains globally traded for large-scale farming and wild populations in some regions.
CONCLUSIONS
We document the dynamic population genetic history of a cosmopolitan dipteran of South American origin shaped by striking geographic patterns. These reflect both ancient dispersal routes, and stochastic and heterogeneous anthropogenic introductions during the last century leading to pronounced diversification of worldwide structure of H. illucens. Upon the recent advent of its agronomic commercialisation, however, current human-mediated translocations of the black soldier fly largely involve genetically highly uniform domesticated strains, which meanwhile threaten the genetic integrity of differentiated unique local resources through introgression. Our in-depth reconstruction of the contemporary and historical demographic trajectories of H. illucens emphasises benchmarking potential for applied future research on this emerging model of the prospering insect-livestock sector.

Identifiants

pubmed: 33952283
doi: 10.1186/s12915-021-01029-w
pii: 10.1186/s12915-021-01029-w
pmc: PMC8101212
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

94

Subventions

Organisme : Bundesamt für Landwirtschaft
ID : 627000824
Organisme : Swiss National Science Foundation
ID : IZ01Z0_147278
Pays : Switzerland
Organisme : Swiss National Science Foundation
ID : 400540_152154
Pays : Switzerland
Organisme : Austrian Science Foundation
ID : FWF P32275
Organisme : Australian Centre for International Agricultural Research
ID : 108866-001
Organisme : National Research Foundation, South Africa
ID : CSRP170506229933

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Auteurs

Cengiz Kaya (C)

Department of Livestock Sciences, Research Institute of Organic Agriculture (FiBL), Frick, Switzerland.
Department of Evolutionary Biology and Environmental Sciences, University of Zurich, Zurich, Switzerland.

Tomas N Generalovic (TN)

Department of Zoology, University of Cambridge, Cambridge, UK.

Gunilla Ståhls (G)

Zoology unit, Finnish Museum of Natural History, Helsinki, Finland.

Martin Hauser (M)

California Department of Food and Agriculture, Plant Pest Diagnostics Branch, Sacramento, USA.

Ana C Samayoa (AC)

Department of Entomology, National Chung Hsing University, Taichung, Taiwan.

Carlos G Nunes-Silva (CG)

Department of Genetics and Biotechnology Graduate Program, Federal University of Amazonas, Manaus, Brazil.

Heather Roxburgh (H)

Biological and Environmental Sciences, University of Stirling, Stirling, UK.

Jens Wohlfahrt (J)

Department of Livestock Sciences, Research Institute of Organic Agriculture (FiBL), Frick, Switzerland.

Ebenezer A Ewusie (EA)

Biotechnology and Nuclear Agriculture Research Institute, Ghana Atomic Energy Commission, Accra, Ghana.

Marc Kenis (M)

CABI, Delémont, Switzerland.

Yupa Hanboonsong (Y)

Department of Entomology, Khon Kaen University, Khon Kaen, Thailand.

Jesus Orozco (J)

Department of Agricultural Sciences and Production, Zamorano University, Zamorano, Honduras.

Nancy Carrejo (N)

Department of Biology, Universidad del Valle, Santiago de Cali, Colombia.

Satoshi Nakamura (S)

Crop, Livestock and Environmental Division, Japan International Research Center for Agricultural Sciences (JIRCAS), Tsukuba, Japan.

Laura Gasco (L)

Department of Agricultural, Forest and Food Sciences, University of Turin, Turin, Italy.

Santos Rojo (S)

Department of Environmental Sciences and Natural Resources, University of Alicante, Alicante, Spain.

Chrysantus M Tanga (CM)

International Centre of Insect Physiology and Ecology (icipe), Nairobi, Kenya.

Rudolf Meier (R)

Department of Biological Sciences, National University of Singapore, Singapore, Singapore.

Clint Rhode (C)

Department of Genetics, Stellenbosch University, Stellenbosch, Republic of South Africa.

Christine J Picard (CJ)

Department of Biology, Indiana University - Purdue University Indianapolis, Indianapolis, USA.

Chris D Jiggins (CD)

Department of Zoology, University of Cambridge, Cambridge, UK.

Florian Leiber (F)

Department of Livestock Sciences, Research Institute of Organic Agriculture (FiBL), Frick, Switzerland.

Jeffery K Tomberlin (JK)

Department of Entomology, Texas A&M University, College Station, USA.

Martin Hasselmann (M)

Department of Livestock Population Genomics, University of Hohenheim, Stuttgart, Germany.

Wolf U Blanckenhorn (WU)

Department of Evolutionary Biology and Environmental Sciences, University of Zurich, Zurich, Switzerland.

Martin Kapun (M)

Department of Evolutionary Biology and Environmental Sciences, University of Zurich, Zurich, Switzerland.
Department of Cell and Developmental Biology, Medical University of Vienna, Vienna, Austria.

Christoph Sandrock (C)

Department of Livestock Sciences, Research Institute of Organic Agriculture (FiBL), Frick, Switzerland. christoph.sandrock@fibl.org.

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