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Cited by 149Genetic diversity and population structureInsect Utilization and EffectsDiptera species taxonomy and behavior

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

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Kaya, Cengiz, Generalovic, Tomas N., Ståhls, Gunilla, Hauser, Martin, Samayoa, Ana C., Nunes-Silva, Carlos G., Roxburgh, Heather, Wohlfahrt, Jens, Ewusie, Ebenezer A., Kenis, Marc, Hanboonsong, Yupa, Orozco, Jesus, Carrejo, Nancy, Nakamura, Satoshi, Gasco, Laura, Rojo, Santos, Tanga, Chrysantus M., Meier, Rudolf, Rhode, Clint, Picard, Christine J., Jiggins, Chris D., Leiber, Florian, Tomberlin, Jeffery K., Hasselmann, Martin, Blanckenhorn, Wolf U., Kapun, Martin, Sandrock, Christoph·2021·BMC Biology
DOI 10.1186/s12915-021-01029-wPMC PMC8101212
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Abstract

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.

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Fig. 1. Global population genetic patterns of Hermetia illucens. Discriminant analysis of principal components depicting all 2862 multilocus genotypes assigned to 16 distinct genetic clusters, independent of the original populations sampled (see also Table 2, Table S6, Additional file 1). a Axes 1 and 2 and b axes 2 and 3. Dots show individuals and numbered labels denote cluster means, both arbitrarily coloured as per the key below panel b. c Posterior probabilities of membership to inferred genetic clusters (K=16) for all individuals (stacked bar plots) arranged as vertical bands within their original populations (Table S3, Additional file 2), indicating admixture proportions with cluster colours as defined in panels a and b. Populations are framed by grey boxes whose widths reflect the number of individuals displayed. The bottom part of panel c shows population grouping according to subcontinental origins using colours that differ from those used for genetic clusters. Population groups labelled with roman numbers refer to major geographic regions and provenances: I: entire Africa—captive; II: west—wild; III: central-east—wild; IV: south-east—wild; V: entire Asia—captive; VI: south-east continental—wild; VII: south-east insular—wild; VIII: west—wild & captive; IX: east—captive; X: southern Polynesia—wild & captive; XI: northern Polynesia—captive; XII: north—wild; XIII: central regions—wild & captive; XIV: south—wild; XV: Caribbean—wild; XVI: entire Europe—captive; XVII: west/central—wild; XVIII: south—wild; XIX: south-east—wild; XX: entire North America—captive; XXI: west—wild; XXII: south-east—wild; XXIII: north-west—wild & captive; XXIV: central-east—wild & captive.
Fig. 1. Global population genetic patterns of Hermetia illucens. Discriminant analysis of principal components depicting all 2862 multilocus genotypes assigned to 16 distinct genetic clusters, independent of the original populations sampled (see also Table 2, Table S6, Additional file 1). a Axes 1 and 2 and b axes 2 and 3. Dots show individuals and numbered labels denote cluster means, both arbitrarily coloured as per the key below panel b. c Posterior probabilities of membership to inferred genetic clusters (K=16) for all individuals (stacked bar plots) arranged as vertical bands within their original populations (Table S3, Additional file 2), indicating admixture proportions with cluster colours as defined in panels a and b. Populations are framed by grey boxes whose widths reflect the number of individuals displayed. The bottom part of panel c shows population grouping according to subcontinental origins using colours that differ from those used for genetic clusters. Population groups labelled with roman numbers refer to major geographic regions and provenances: I: entire Africa—captive; II: west—wild; III: central-east—wild; IV: south-east—wild; V: entire Asia—captive; VI: south-east continental—wild; VII: south-east insular—wild; VIII: west—wild & captive; IX: east—captive; X: southern Polynesia—wild & captive; XI: northern Polynesia—captive; XII: north—wild; XIII: central regions—wild & captive; XIV: south—wild; XV: Caribbean—wild; XVI: entire Europe—captive; XVII: west/central—wild; XVIII: south—wild; XIX: south-east—wild; XX: entire North America—captive; XXI: west—wild; XXII: south-east—wild; XXIII: north-west—wild & captive; XXIV: central-east—wild & captive.CC BY · PubMed Central
Fig. 2. Factorial correspondence analysis (FCA) of 150 Hermetia illucens populations. Population ‘barycentres’ labelled according to provenance status and subcontinent of origin are projected in multidimensional space based on FCA axes 1 and 2 (panel a) and axes 2 and 3 (panel b), which together explain 22.2% of the total variance. Individual-based multivariate ordination according to population provenance nested within subcontinent is shown as a complementary analysis in Figure S4, Additional file 2.
Fig. 2. Factorial correspondence analysis (FCA) of 150 Hermetia illucens populations. Population ‘barycentres’ labelled according to provenance status and subcontinent of origin are projected in multidimensional space based on FCA axes 1 and 2 (panel a) and axes 2 and 3 (panel b), which together explain 22.2% of the total variance. Individual-based multivariate ordination according to population provenance nested within subcontinent is shown as a complementary analysis in Figure S4, Additional file 2.CC BY · PubMed Central
Fig. 3. Dendrogram of Cavalli-Sforza and Edwards chord distances of 150 Hermetia illucens populations. Population cluster allocations (based on the majority of assigned individuals) are gradient-highlighted in the background according to Fig. 1. For some highly admixed populations, the second-most abundant clusters are indicated in a separate column. Labels at the branch-tips represent population provenances and subcontinental origins as defined in Fig. 2. Additional information on major geographic regions of origin is specified for wild populations and selected strains (see Table 2)
Fig. 3. Dendrogram of Cavalli-Sforza and Edwards chord distances of 150 Hermetia illucens populations. Population cluster allocations (based on the majority of assigned individuals) are gradient-highlighted in the background according to Fig. 1. For some highly admixed populations, the second-most abundant clusters are indicated in a separate column. Labels at the branch-tips represent population provenances and subcontinental origins as defined in Fig. 2. Additional information on major geographic regions of origin is specified for wild populations and selected strains (see Table 2)CC BY · PubMed Central
Fig. 4. Inferred global distribution dynamics of Hermetia illucens genetic clusters. Pie charts represent proportions of individuals sampled in major geographic regions and assigned to genetic clusters according to Fig. 1 (see also Table 2 and Table S6, Additional file 2). Pie diameters correspond to sample sizes and pies comprising multiple samples reflect whole regions (see Table S10, Additional file 2, for more detail). a Map depicting biogeographically informative wild and/or captive populations as indicated according to the symbols plotted on starting points referring to major geographic regions. Colonisation routes, as inferred from ABC analyses (Figure S6, Tables S11-13, Additional file 2), are indicated by schematically simplified trajectories. Indigenous range expansions are shown by solid arrows and dispersal to non-native regions are differentiated to show founder events from single sources (dashed-dotted arrows), admixture between demographically independent introductions (dashed arrows), and serial colonisations (dotted arrows). Origins mostly refer to whole regions rather than specific locations. b Map depicting exclusively captive population pools from entire continents of North America, Europe, Africa and Asia, and inferred major trading directions of domesticated strains and their introgressants of clusters 1–5 (see Table S10, Additional file 2, and main text for more detail)
Fig. 4. Inferred global distribution dynamics of Hermetia illucens genetic clusters. Pie charts represent proportions of individuals sampled in major geographic regions and assigned to genetic clusters according to Fig. 1 (see also Table 2 and Table S6, Additional file 2). Pie diameters correspond to sample sizes and pies comprising multiple samples reflect whole regions (see Table S10, Additional file 2, for more detail). a Map depicting biogeographically informative wild and/or captive populations as indicated according to the symbols plotted on starting points referring to major geographic regions. Colonisation routes, as inferred from ABC analyses (Figure S6, Tables S11-13, Additional file 2), are indicated by schematically simplified trajectories. Indigenous range expansions are shown by solid arrows and dispersal to non-native regions are differentiated to show founder events from single sources (dashed-dotted arrows), admixture between demographically independent introductions (dashed arrows), and serial colonisations (dotted arrows). Origins mostly refer to whole regions rather than specific locations. b Map depicting exclusively captive population pools from entire continents of North America, Europe, Africa and Asia, and inferred major trading directions of domesticated strains and their introgressants of clusters 1–5 (see Table S10, Additional file 2, and main text for more detail)CC BY · PubMed Central

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Research works printed but not linked: 5

  1. Kupferschmidt K. Buzz Food. Science. 2015;350:267–9.
  2. Sandrock C, Leupi S, Wohlfahrt J, Leiber F, Kreuzer M. Genotype × environment interactions in black soldier fly larvae grown on different feed substrates. 70th Annual Meeting of the European Federation of Animal Science. Ghent: Wageningen Academic publishers; 2019. p. 239.
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Metadata

Authors
Kaya, C., Generalovic, T. N., Ståhls, G., Hauser, M., Samayoa, A. C., Nunes-Silva, C. G., Roxburgh, H., Wohlfahrt, J., Ewusie, E. A., Kenis, M., Hanboonsong, Y., Orozco, J., Carrejo, N., Nakamura, S., Gasco, L., Rojo, S., Tanga, C. M., Meier, R., Rhode, C., Picard, C. J., Jiggins, C. D., Leiber, F., Tomberlin, J. K., Hasselmann, M., Blanckenhorn, W. U., Kapun, M., & Sandrock, C.
Affiliations
  • University of Zurich (CH)
  • University of Cambridge (GB)
  • Finnish Museum of Natural History (FI)
  • California Department of Food and Agriculture (US)
  • National Chung Hsing University (TW)
  • Universidade Federal do Amazonas (BR)
  • University of Stirling (GB)
  • Forschungsinstitut für Biologischen Landbau (CH)
  • Ghana Atomic Energy Commission (GH)
  • CABI Switzerland (CH)
  • Khon Kaen University (TH)
  • Universidad del Valle (CO)
  • Japan International Research Center for Agricultural Sciences (JP)
  • University of Turin (IT)
  • University of Alicante (ES)
  • International Centre of Insect Physiology and Ecology (KE)
  • National University of Singapore (SG)
  • Stellenbosch University (ZA)
  • Indiana University Indianapolis (US)
  • Texas A&M University (US)
  • University of Hohenheim (DE)
Corresponding author
Sandrock, Christoph
ORCID
Venue
BMC Biology
Publisher
Springer Science and Business Media LLC
Published
2021-05-05
Volume
19
Issue
1
Pages
94-94
ISSN
1741-7007 (ISSN-L)
DOI
10.1186/s12915-021-01029-w
PMC
PMC8101212
OpenAlex
W3157995364
Cited by
149
References
135
Citations by year
2026: 29 · 2025: 34 · 2024: 29 · 2023: 21 · 2022: 26 · 2021: 10
FWCI
12.16
Type
journal article
Language
en
Open access
Licence
Locations
  • BMC Biology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, cc-by)
  • IUScholarWorks (Indiana University) (submittedVersion, cc-by)
  • Työväentutkimus Vuosikirja (submittedVersion)
  • Institutional Research Information System University of Turin (University of Turin) (submittedVersion, other-oa)
  • SUNScholar (Stellenbosch University) (submittedVersion)
  • National University of Singapore (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Stirling Online Research Repository (University of Stirling) (submittedVersion, cc-by)
  • RUA, Repositorio Institucional de la Universidad de Alicante (Universidad de Alicante) (submittedVersion, cc-by)
  • Apollo (University of Cambridge) (submittedVersion, cc-by)
  • Zurich Open Repository and Archive (University of Zurich) (submittedVersion, cc-by)
  • Apollo
  • Apollo (cc-by)
  • Zurich Open Repository and Archive (University of Zurich)
Funders
  • Bundesamt für Landwirtschaft (627000824)
  • Swiss National Science Foundation (IZ01Z0_147278, 400540_152154)
  • Austrian Science Foundation (FWF P32275)
  • Australian Centre for International Agricultural Research (108866-001)
  • National Research Foundation, South Africa (CSRP170506229933)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect Utilization and Effects
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Diptera species taxonomy and behavior
Keywords
Hermetia illucens, population structure, demographic history, microsatellite markers, domestication, introgression, invasive species, range expansion, founder events, genetic diversity, insect farming, organic waste bioconversion, captive populations
MeSH terms
Animals, Animal Feed, Demography, Diptera, Genetics, Population, Humans, Larva

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