Genetic Diversity and Phylogeographic Structure of the Edible Caterpillars of Gynanisa maja and Implications for the Sustainability of the Species in Namibia

Zwannda Nethavhani , William Versfeld , Ruan Veldtman , Barbara van Asch

Integrative Conservation ›› 2025, Vol. 4 ›› Issue (3) : 405 -415.

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Integrative Conservation ›› 2025, Vol. 4 ›› Issue (3) : 405 -415. DOI: 10.1002/inc3.70029
RESEARCH ARTICLE

Genetic Diversity and Phylogeographic Structure of the Edible Caterpillars of Gynanisa maja and Implications for the Sustainability of the Species in Namibia

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Abstract

Caterpillars of Gynanisa maja (Lepidoptera: Saturniidae) are extensively harvested from the wild for human consumption across their geographic range in southern Africa. Although concerns have been raised on the sustainability of this practice in the current scenario of habitat loss and climate change, genetic data for assessments of the phylogeographic structure, genetic diversity, and demographic history of the species is severely lacking. This study presents the first insights into these aspects of Gy. maja populations in Namibia using mitochondrial sequence data. Adult specimens and caterpillars (n = 72) were collected at six sampling areas in the northwestern Namibia for Sanger sequencing of polymorphic mitochondrial regions (1964 bp) followed by haplotype-based analyses. The phylogeographic structure of Gy. maja was assessed using a phylogenetic tree and neighbour-joining networks, along with estimates of genetic diversity and demographic history. We found a total of 47 haplotypes, with only a few shared haplotypes among sampling areas. Standard genetic diversity measures showed high levels of haplotype and nucleotide diversity at all sampling sites. Neutrality tests, mismatch distributions and raggedness index indicate a stationary population. Overall, our results suggest that Gy. maja in northwestern Namibia is genetically diverse and panmictic, and that the genetic diversity and demographic status of the species are presently not of immediate concern. However, it is worth noting that dry mopane woodlands, the main habitat of Gy. maja in Namibia, are under increasing anthropogenic pressure that will inevitably impact the health and abundance of these and other edible Lepidoptera, especially those harvested at commercial scale.

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African Saturniidae / genetic diversity / mitochondrial / phylogenetics / phylogeography

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Zwannda Nethavhani, William Versfeld, Ruan Veldtman, Barbara van Asch. Genetic Diversity and Phylogeographic Structure of the Edible Caterpillars of Gynanisa maja and Implications for the Sustainability of the Species in Namibia. Integrative Conservation, 2025, 4(3): 405-415 DOI:10.1002/inc3.70029

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References

[1]

Alvarado Bremer, J. R., J. Viñas, J. Mejuto, B. Ely, and C. Pla. 2005. “Comparative Phylogeography of Atlantic Bluefin Tuna and Swordfish: The Combined Effects of Vicariance, Secondary Contact, Introgression, and Population Expansion on the Regional Phylogenies of Two Highly Migratory Pelagic Fishes.” Molecular Phylogenetics and Evolution 36: 169–187. https://doi.org/10.1016/j.ympev.2004.12.011.

[2]

Badanaro, F., K. Amevoin, C. Lamboni, and K. Amouzou. 2014. “Edible Cirina forda (Westwood, 1849) (Lepidoptera: Saturniidae) Caterpillar Among Moba People of the Savannah Region in North Togo: From Collector to Consumer.” Asian Journal of Applied Science and Engineering 3: 13–24. https://doi.org/10.15590/ajase/2014/v3i8/54479.

[3]

Baiyegunhi, L. J. S., and B. B. Oppong. 2016. “Commercialisation of Mopane Worm (Imbrasia belina) in Rural Households in Limpopo Province, South Africa.” Forest Policy and Economics 62: 141–148. https://doi.org/10.1016/j.forpol.2015.08.012.

[4]

Baiyegunhi, L. J. S., B. B. Oppong, and M. G. Senyolo. 2016. “Socio-Economic Factors Influencing Mopane Worm (Imbrasia belina) Harvesting in Limpopo Province, South Africa.” Journal of Forestry Research 27: 443–452. https://doi.org/10.1007/s11676-015-0168-z.

[5]

Bandelt, H. J., P. Forster, and A. Rohl. 1999. “Median-Joining Networks for Inferring Intraspecific Phylogenies.” Molecular Biology and Evolution 16: 37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036.

[6]

Chanda, B., C. Olweny, and D. Chungu. 2021. “Forage Preference Identification of Wild Gynanisa maja (Klug, 1836) and Perspectives for Improved Livelihoods in Zambia.” Journal of Insects as Food and Feed 7: 99–108.

[7]

Eisenhauer, N., A. Bonn, and C. A. Guerra. 2019. “Recognizing the Quiet Extinction of Invertebrates.” Nature Communications 10: 50. https://doi.org/10.1038/s41467-018-07916-1.

[8]

Excoffier, L.2004. “Patterns of Dna Sequence Diversity and Genetic Structure After a Range Expansion: Lessons From the Infinite-Island Model.” Molecular Ecology 13: 853–864. https://doi.org/10.1046/j.1365-294X.2003.02004.x.

[9]

Excoffier, L., and H. E. L. Lischer. 2010. “Arlequin Suite Ver 3.5: A New Series of Programs to Perform Population Genetics Analyses Under Linux and Windows.” Molecular Ecology Resources 10: 564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x.

[10]

Excoffier, L., P. E. Smouse, and J. M. Quattro. 1992. “Analysis of Molecular Variance Inferred From Metric Distances Among DNA Haplotypes: Application to Human Mitochondrial DNA Restriction Data.” Genetics 131: 479–491. https://doi.org/10.1093/genetics/131.2.479.

[11]

Fu, Y. X.1997. “Statistical Tests of Neutrality of Mutations Against Population Growth, Hitchhiking and Background Selection.” Genetics 147: 915–925. https://doi.org/10.1093/genetics/147.2.915.

[12]

Green, M. R., and J. Sambrook. 2017. “Isolation of High-Molecular-Weight DNA Using Organic Solvents.” Cold Spring Harbor Protocols 2017: 356–359. https://doi.org/10.1101/pdb.prot093450.

[13]

Guindon, S., J. F. Dufayard, V. Lefort, M. Anisimova, W. Hordijk, and O. Gascuel. 2010. “New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0.” Systematic Biology 59: 307–321. https://doi.org/10.1093/sysbio/syq010.

[14]

Hallmann, C. A., M. Sorg, E. Jongejans, et al. 2017. “More Than 75 Percent Decline Over 27 Years in Total Flying Insect Biomass in Protected Areas.” PLoS One 12: e0185809. https://doi.org/10.1371/journal.pone.0185809.

[15]

Harpending, H. C.1994. “Signature of Ancient Population Growth in a Low-Resolution Mitochondrial DNA Mismatch Distribution.” Human Biology 66: 591–600.

[16]

Hebert, P. D. N., E. H. Penton, J. M. Burns, D. H. Janzen, and W. Hallwachs. 2004. “Ten Species in One: DNA Barcoding Reveals Cryptic Species in the Neotropical Skipper Butterfly Astraptes fulgerator.” Proceedings of the National Academy of Sciences 101: 14812–14817. https://doi.org/10.1073/pnas.0406166101.

[17]

Hlongwane, Z. T., R. Slotow, and T. C. Munyai. 2020. “Nutritional Composition of Edible Insects Consumed in Africa: A Systematic Review.” Nutrients 12: 2786. https://doi.org/10.3390/nu12092786.

[18]

Hoang, D. T., O. Chernomor, A. Von Haeseler, B. Q. Minh, and L. S. Vinh. 2018. “UFBoot2: Improving the Ultrafast Bootstrap Approximation.” Molecular Biology and Evolution 35: 518–522. https://doi.org/10.1093/molbev/msx281.

[19]

Hope, R. A., P. G. H. Frost, A. Gardiner, and J. Ghazoul. 2009. “Experimental Analysis of Adoption of Domestic Mopane Worm Farming Technology in Zimbabwe.” Development Southern Africa 26: 29–46. https://doi.org/10.1080/03768350802640065.

[20]

Katoh, K., and D. M. Standley. 2013. “MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability.” Molecular Biology and Evolution 30: 772–780. https://doi.org/10.1093/molbev/mst010.

[21]

Kim, S. R., K. Y. Kim, J. S. Jeong, et al. 2017. “Population Genetic Characterization of the Japanese Oak Silkmoth, Antheraea yamamai (Lepidoptera: Saturniidae), Using Novel Microsatellite Markers and Mitochondrial DNA Gene Sequences.” Genetics and Molecular Research 16: 2. https://doi.org/10.4238/gmr16029608.

[22]

Kusia, E. S., C. Borgemeister, F. M. Khamis, et al. 2021. “Diversity, Host Plants and Potential Distribution of Edible Saturniid Caterpillars in Kenya.” Insects 12: 600. https://doi.org/10.3390/insects12070600.

[23]

Langley, J., S. Van der Westhuizen, G. Morland, and B. van Asch. 2020. “Mitochondrial Genomes and Polymorphic Regions of Gonimbrasia belina and Gynanisa maja (Lepidoptera: Saturniidae), Two Important Edible Caterpillars of Southern Africa.” International Journal of Biological Macromolecules 144: 632–642. https://doi.org/10.1016/j.ijbiomac.2019.12.055.

[24]

Lautenschläger, T., C. Neinhuis, M. Monizi, et al. 2017. “Edible Insects of Northern Angola.” African Invertebrates 58: 55–82. https://doi.org/10.3897/AfrInvertebr.58.21083.

[25]

Marí-Mena, N., C. Lopez-Vaamonde, H. Naveira, M. A. Auger-Rozenberg, and M. Vila. 2016. “Phylogeography of the Spanish Moon Moth Graellsia isabellae (Lepidoptera, Saturniidae).” BMC Evolutionary Biology 16: 139. https://doi.org/10.1186/s12862-016-0708-y.

[26]

Men, Q., G. Xue, D. Mu, Q. Hu, and M. Huang. 2017. “Mitochondrial DNA Markers Reveal High Genetic Diversity and Strong Genetic Differentiation in Populations of Dendrolimus kikuchii Matsumura (Lepidoptera: Lasiocampidae).” PLoS One 12: e0179706. https://doi.org/10.1371/journal.pone.0179706.

[27]

Mogomotsi, P. K., G. E. Mogomotsi, and R. Gondo. 2018. “Utilisation of Non-Timber Forest Products in Botswana: The Case of Commercialisation of Mopane Worms (Imbraisia belina) in Central District, Botswana'.” Journal of Forestry and Environmental Science 34: 24–30.

[28]

Ndlovu, I., W. N. Nunu, N. Mudonhi, O. Dube, and A. Maviza. 2019. “Land Use−Land Cover Changes and Mopani Worm Harvest in Mangwe District in Plumtree, Zimbabwe.” Environmental Systems Research 8: 11. https://doi.org/10.1186/s40068-019-0141-5.

[29]

Nemadodzi, L. E., G. M. Managa, and G. Prinsloo. 2023. “The Use of Gonimbrasia belina (Westwood, 1849) and Cirina Forda (Westwood, 1849) Caterpillars (Lepidoptera: Sarturniidae) as Food Sources and Income Generators in Africa.” Foods 12: 2184. https://doi.org/10.3390/foods12112184.

[30]

Nethavhani, Z., R. Straeuli, K. Hiscock, et al. 2022. “Mitogenomics and Phylogenetics of Twelve Species of African Saturniidae (Lepidoptera).” PeerJ 10: e13275. https://doi.org/10.7717/peerj.13275.

[31]

Nethavhani, Z., R. Veldtman, C. Nyamukondiwa, W. Versfeld, and B. van Asch. 2025. “Multimarker Genetic Analyses of Gonimbrasia belina, the Most Harvested Wild Edible Insect of Mopane Woodlands in Southern Africa, Supports Concerns Over the Sustainability of the Species.” Conservation Genetics 26: 545–559. https://doi.org/10.1007/s10592-025-01687-1.

[32]

Nguyen, L. T., H. A. Schmidt, A. Von Haeseler, and B. Q. Minh. 2015. “IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies.” Molecular Biology and Evolution 32: 268–274. https://doi.org/10.1093/molbev/msu300.

[33]

Numbi Muya, G. M., B. K. Mutiaka, J. Bindelle, F. Francis, and R. Caparros Megido. 2022. “Human Consumption of Insects in Sub-Saharan Africa: Lepidoptera and Potential Species for Breeding.” Insects 13: 886. https://doi.org/10.3390/insects13100886.

[34]

Oberprieler, R. G. 1995. The Emperor Moths of Namibia. Ekogilde.

[35]

QGIS Development Team. 2023. QGIS Geographic Information System.

[36]

R Core Team. 2021. R: A Language and Environment for Statistical Computing.

[37]

Ramos-Onsins, S. E., and J. Rozas. 2002. “Statistical Properties of New Neutrality Tests Against Population Growth.” Molecular Biology and Evolution 19: 2092–2100. https://doi.org/10.1093/oxfordjournals.molbev.a004034.

[38]

Rozas, J., A. Ferrer-Mata, J. C. Sánchez-Delbarrio, et al. 2017. “DnaSP 6: DNA Sequence Polymorphism Analysis of Large Data Sets.” Molecular Biology and Evolution 34: 3299–3302. https://doi.org/10.1093/molbev/msx248.

[39]

Sekonya, J. G., N. J. McClure, and R. P. Wynberg. 2020. “New Pressures, Old Foodways: Governance and Access to Edible Mopane Caterpillars, Imbrasia (=Gonimbrasia) Belina, in the Context of Commercialization and Environmental Change in South Africa.” International Journal of the Commons 14: 139–153. https://doi.org/10.5334/ijc.978.

[40]

Smith, A. K., B. Slippers, B. P. Hurley, and G. Fourie. 2022. “Diversity of Lepidoptera Associated With Macadamia Nut Damage in South Africa and Development of Molecular Tools to Monitor Pest Populations.” Agricultural and Forest Entomology 24: 332–343. https://doi.org/10.1111/afe.12497.

[41]

de Swardt, D. B., C. Wigley-Coetsee, and T. G. O'Connor. 2018. “Insect Outbreaks Alter Nutrient Dynamics in a Southern African Savanna: Patchy Defoliation of Colophospermum Mopane Savanna by Imbrasia belina Larvae.” Biotropica 50: 789–796. https://doi.org/10.1111/btp.12565.

[42]

Tajima, F.1989. “The Effect of Change in Population Size on DNA Polymorphism.” Genetics 123: 597–601. https://doi.org/10.1093/genetics/123.3.597.

[43]

Thomas, B.2013. “Sustainable Harvesting and Trading of Mopane Worms (Imbrasia belina) in Northern Namibia: An Experience From the Uukwaluudhi Area.” International Journal of Environmental Studies 70: 494–502. https://doi.org/10.1080/00207233.2013.829324.

[44]

Togarepi, C., E. Nashidengo, and N. Siyambango. 2020. “Effects of Climatic Variability and Non-Climatic Factors on Mopane Worms' (Gonimbrasia belina) Distribution and Livelihood Options in North Central Namibia.” Environment and Natural Resources Research 10: 14. https://doi.org/10.5539/enrr.v10n2p14.

[45]

Turner, W. C., S. Périquet, and C. E. Goelst, et al. 2022. “Africa's Drylands in a Changing World: Challenges for Wildlife Conservation Under Climate and Land-Use Changes in the Greater Etosha Landscape. Glob.” Ecology and Conservation 38: 1–28. https://doi.org/10.1016/j.gecco.2022.e0221.

[46]

van Voorthuizen, E. G.1976. “The Mopane Tree.” Botswana Notes and Records 8: 223–230.

[47]

Wei, S. J., B. C. Shi, Y. J. Gong, et al. 2013. “Genetic Structure and Demographic History Reveal Migration of the Diamondback Moth Plutella xylostella (Lepidoptera: Plutellidae) From the Southern to Northern Regions of China.” PLoS One 8: 1–14. https://doi.org/10.1371/journal.pone.0059654.

[48]

Wright, S.1949. “The Genetical Structure of Populations.” Annals of Eugenics 15: 323–354. https://doi.org/10.1111/j.1469-1809.1949.tb02451.x.

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2025 The Author(s). Integrative Conservation published by John Wiley & Sons Australia, Ltd on behalf of Xishuangbanna Tropical Botanical Garden (XTBG).

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