Procruste analysis of forewing shape in two endemic honeybee subspecies Apis mellifera intermissa and A. m. sahariensis from the Northwest of Algeria
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Abstract. Abed F, Bachir-Bouiadjra B, Dahloum L, Yakubu A, Haddad A, Homrani A. 2021. Procruste analysis of forewing shape in two endemic honeybee subspecies Apis mellifera intermissa and A. m. sahariensis from the Northwest of Algeria. Biodiversitas 22: 154-164. Honey bees play an important role as pollinators of many crops. Thus they are collectively considered as a veritable economic source. The present study was undertaken to describe variation in the right forewing geometry in two Algerian honeybee subspecies Apis mellifera intermissa and Apis mellifera sahariensis using landmark-based geometric morphometrics. A total of 1286 honeybees were sampled from 12 provinces in the northwest of Algeria. The forewing geometry was evaluated using 20 homologous landmarks by applying Procrustes superimposition analysis. The top four principal components accounted for only 41.1% of wing shape variation between the two subspecies. There was a significant difference in wing shape between the two subspecies (Mahalanobis distance = 1.0626 ; P<0.001), whereas their wing size seemed similar (P>0.05). Regarding the allometric effect, the percentage of variation in wing shape explained by size changes was relatively small, with 1.28% and 4.37% for A. m. intermissa and A.m sahariensis, respectively. The cross-validation procedure correctly classified 68.3% of specimens into their original groups. PERMANOVA test revealed significant differences in the right forewing shape among all geographic areas studied (P<0.001). The results clearly showed that the landmark-based geometric approach applied to forewings venation is a powerful and reliable tool in the discrimination of native honey bee subspecies and should be considered in local honey bee biodiversity improvement and conservation initiatives.
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References
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Dolati L, NazemiRa?e J, Khalesro H. 2013. Landmark-based morphometric study in the fore and hind wings of an Iranian Race of European honeybee (Apis mellifera meda). J Apic Sci (57) : 187–197.
Doornik JA, Hansen H. 2008. An omnibus test for univariate and multivariate normality. Oxf Bull Econ Stat 70: 927–939.
Fagundes J, Rebelo A, Digiampietri L, e Bíscaro H. 2020. Fully automatic segmentation of bee wing images. Revista Brasileira de Computação Aplicada 12 (2) : 37-45. DOI : 10.5335/rbca.v12i2.10420.
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Francoy TM, Faria Franco F, Roubik DW. 2012. Integrated landmark and outline-based morphometric methods efficiently distinguish species of Euglossa (Hymenoptera, Apidae, Euglossini). Apidologie (Celle) 43: 609–617. DOI : 10.1007/s13592-012-0132-2
Gonçalves PHP. 2010. Análise da variabilidade de uma pequena população de Frieseomelitta varia (Hymenoptera, Apidae, Meliponini), pormeio de análise do DNA mitocondrial, microddatélites e morfometria geométrica das asas. Dissertação de Mestrado, Universidade de São Paulo, São Paulo–SP. 140 p.
Hammer, Øyvind, Harper, David AT, Paul D, Ryan. 2001. Past: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontol. Electron 4 (1), art. 4: 9 pp. 178kb.
Henriques D, Chávez-Galarza J, Teixeira JSG, Ferreira H, Neves CJ, Francoy TM, Pinto MA. 2020. Wing geometric morphometrics of workers and drones and single nucleotide polymorphisms provide similar genetic structure in the Iberian honey bee (Apis mellifera iberiensis). Insects 11 (2): 89. DOI :10.3390/insects11020089.
Kandemir I, Özkan A, Fuchs S. 2011. Reevaluation of honeybee (Apis mellifera) microtaxonomy: a geometric morphometric approach. Apidologie (Celle) 42: 618–627. DOI: 10.1007/ s13592-011-0063-3
Klingenberg CP. 2011. MorphoJ: An integrated software package for geometric morphometrics. Mol Ecol Resour (11) : 353–357.
Leonidas C, Fani H, Maria B, Mica M, Anastasios DM. 2014. Morphological discrimination of greek honeybee populations based on geometric morphometrics analysis of wing shape. J Apic Sci 58 (1). DOI : 10.2478/JAS- 2014-000.
Marghitas AL, Paniti-Teleky O, Dezmirean D, Rodica M, Cristina B, Coroian C, Laura L, Adela M. 2008. Morphometric differences between honeybees (Apis mellifera carpatica) Populations from Transylvanian area, Scientific Papers Animal Science and Biotechnologies 41 (2): 309-315
Miguel I, Baylac M, Iriondo M, Manzano C, Garney L, Estonba A. 2011. Both geometric morphometrics and microsatellite data support the differenciation of the Apis mellifera M evolutionary branch. Apidologie (Celle) 42 (2): 150–161. DOI : 10.1051/apido/2010048.
Nawrocka A, Kandemir ?, Fuchs S, Tofilski A. 2018. Computer software for identification of honey bee subspecies and evolutionary lineages. Apidologie (Celle) 49: 172–184. DOI : 10.1007/s13592-017-0538-y. DOI : 10.1007/s13592-017-0538-y
Oleksa A, To?lski A. 2014. Wing geometric morphometrics and microsatellite analysis provide similar discrimination of Honey Bee subspecies. Apidologie (Celle) 46: 49–60. DOI : 10.1007/s13592-014-0300-7
Outomuro D, Johansson FA. 2017. Potential pitfall in studies of biological shape: Does size matter ?. J Anim Ecol 86: 1447–1457. DOI : 10.1111/1365- 2656.12732.
Pavlinov IY. 2001. Geometric morphometrics, a new analytical approach to comparision of digitized images. Information Technology in Biodiversity Research: Abstracts of the 2nd International Symposium. St. Petersburg: Russian Academy of Science, 44–64.
Prado-Silva A, Nunes LA, De Oliveira Alves RM, Carneiro PLS, Waldschmidt AM. 2016. Variation of fore wing shape in Melipona mandacaia Smith, 1863 (Hymenoptera, Meliponini) along its geographic range. J Hymenopt Res 48: 85-94. DOI : 10.3897/JHR.48.6619.
Rohlf FJ. 2001. TPS Dig 2.16 software. State University of New York at Stony Brook, NY
Rohlf FJ. 2017. tpsRelw-relative warp analysis, version 1.67. New York (NY): Stony Brook University, Stony Brook.
Rohlf FJ. 2017. Tps Utility program, Version 1.74. Ecology and Evolution and Anthropology, Stony Brook University
Ruttner F. 1988. Biogeography and Taxonomy of Honeybees. Springer, Berlin.
Sandoval Ramirez CM, Nieves Blanco EE, Gutiérrez Marin R, Jaimes Mendez DA, Rodríguez NO, Otálora-Luna F, Aldana, E. J. 2015. Morphometric analysis of the host effect on phenotypical variation of Belminus ferroae (Hemiptera: Triatominae). Psyche, 1–12. DOI : 10.1155/2015/613614
Salehi, S, Nazemi-Rafie, J. 2020. Discrimination of Iranian honeybee populations (Apis mellifera meda) from commercial subspecies of Apis mellifera L. using morphometric and genetic methods. J Asia Pac Entomol, 23, 591-598. DOI : 10.1016/j.aspen.2020.04.009
Silva F. 2015. Automated Bee Species Identification Through Wing Images. [Thesis]. University of Sao Paulo, [Brazilian].
Skandalis DA, Segre PS, Bahlman JW, Groom DJE, Welch Jr, KCW, Witt CC, McGuire JA, Dudley R, Lentink D, Altshuler DL. 2017. The biomechanical origin of extreme wing allometry in humming birds. Nat Commun 8, 1047. DOI : 10.1038/s41467-017-01223-x
Slice DE. 2002. Morpheus, For morphometric research software. Department of Biomedical Engineering, Wake Forest University School of Medicine, Winston, Salem.
Sontigun N, Sukontason KL, Zajac B, Zehner R, Sukontason K, Wannasan A, Amendt J. 2017. Wing morphometrics as a tool in species identification of forensically important blow flies of Thailand. Parasit Vectors 10:229. DOI :10.1186/s13071-017-2163-z
Sultan AA. 2015. Studying the variation of wing shape and size for Iraqi honey bee worker apis mellifera (Hymenoptera : Apidae) collected from Baghdad and Diyala provinces by using geometric morphometric of wing. Int J Curr Res 7 (1), pp.11319- 11324.
Tatsuta H, Takahashi KH, Sakamaki Y. 2018. Geometric morphometrics in entomology: Basics and applications. Entomol Sci 21 (2): 164–184. DOI : 10.1111/ens.12293. DOI : 10.1111/ens.12293
Tofilski A. 2008. Using geometric morphometrics and standard morphometry to discriminate three honeybee subspecies. Apidologie (Celle) 39: 558–563. DOI: 10.1051/apido:2008037
Townsend CR, Begon M, Harper JL. 2008. Essentials of Ecology. 3rd Edition. Wiley-Blackwell, Oxford.
Arias MC, Rinderer TE, Sheppard WS. 2006. Further characterization of honeybees from the Iberian peninsula by allozyme, morphometric and mtDNA haplotype analyses. J Apic Res. 45 (4): 188-196.
Atsalek R, Chanpen C, Siriwat W. 2012. Geometric morphometric analysis of giant honeybee (Apis dorsata Fabricius, 1793) populations in Thailand. J Asi. Pac Entomol 15 (4): 611-618.
Baleba SBS, Masiga D, Torto B et al. 2019. Effect of larval density and substrate quality on the wing geometry of Stomoxys calcitrans L. (Diptera: Muscidae). Parasit Vectors 12: 222. DOI : 10.1186/s13071-019-3483-y.
Barour C, Baylac M. 2016. Geometric morphometric discrimination of the three African honeybee subspecies Apis mellifera intermissa, A. m. sahariensis and A. m. capensis (Hymenoptera, Apidae): Fore wing and hind wing landmark configurations. J Hymenopt Res 52, 61–70. DOI :10.3897/jhr.52.8787
Barour C, Tahar A, Baylac M. 2011. Forewing shape variation in Algerian honeybee populations of Apis mellifera intermissa (Buttel-Reepen, 1906) (Hymenoptera: Apidae): A landmark based geometric morphometrics analysis. Afr. Entomol 19(1): 11–22. DOI : 10.4001/003.019.0101
Bookstein FL. 1991. Morphometric tools for landmark data: geometry and biology. Cambridge University Press, New York : 435 pp.
Bustamante T, Baiser B, Ellis JD. 2020. Comparing classical and geometric morphometric methods to discriminate between the South African honey bee subspecies Apis mellifera scutellata and Apis mellifera capensis (Hymenoptera: Apidae). Apidologie (Celle) 51: 123–136. DOI : 10.1007/s13592-019-00651-6.
Coroian CO, Muñoz I, Schlüns EA, Paniti?Teleky OR, Erler S, Furdui EM, M?rghita? LA, Dezmirean DS, Schlüns H, De la Rúa P, Moritz RFA. 2014. Climate rather than geography separates two European honeybee subspecies. Mol Ecol 23 (9), 2353-2361. DOI :10.1111/mec.12731.
Cristovam ALJ, Carlos ALC, Lorena AN, Tiago MF. 2012. Population Divergence of Melipona scutellaris (Hymenoptera: Meliponina) in Two Restricted Areas in Bahia, Brazil. Sociobiology. DOI : 10.13102/sociobiology.v59i1.670.
Dellicour S, Gerard M, Prunier JG, Dewulf A, Kuhlmann M, Michez D. 2017. Distribution and predictors of wing shape and size variability in three sister species of solitary bees. PloS One 12 (3), e0173109. DOI : 10.1371/journal.pone.0173109.
DeVries PJ, Penz CM, Hill RI. 2010. Vertical distribution, flight behaviour and evolution of wing morphology in Morpho butterflies: wing evolution in Morpho butterflies. J Anim Ecol 79:1077–85.
Dolati L, NazemiRa?e J, Khalesro H. 2013. Landmark-based morphometric study in the fore and hind wings of an Iranian Race of European honeybee (Apis mellifera meda). J Apic Sci (57) : 187–197.
Doornik JA, Hansen H. 2008. An omnibus test for univariate and multivariate normality. Oxf Bull Econ Stat 70: 927–939.
Fagundes J, Rebelo A, Digiampietri L, e Bíscaro H. 2020. Fully automatic segmentation of bee wing images. Revista Brasileira de Computação Aplicada 12 (2) : 37-45. DOI : 10.5335/rbca.v12i2.10420.
Francoy TM, Imperatriz-Fonseca VL. 2010. A morfometria geométricade asas e a identifiação automática de espécies de abelhas. Oecologia Aust 14 (1): 317-321.
Francoy TM, Faria Franco F, Roubik DW. 2012. Integrated landmark and outline-based morphometric methods efficiently distinguish species of Euglossa (Hymenoptera, Apidae, Euglossini). Apidologie (Celle) 43: 609–617. DOI : 10.1007/s13592-012-0132-2
Gonçalves PHP. 2010. Análise da variabilidade de uma pequena população de Frieseomelitta varia (Hymenoptera, Apidae, Meliponini), pormeio de análise do DNA mitocondrial, microddatélites e morfometria geométrica das asas. Dissertação de Mestrado, Universidade de São Paulo, São Paulo–SP. 140 p.
Hammer, Øyvind, Harper, David AT, Paul D, Ryan. 2001. Past: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontol. Electron 4 (1), art. 4: 9 pp. 178kb.
Henriques D, Chávez-Galarza J, Teixeira JSG, Ferreira H, Neves CJ, Francoy TM, Pinto MA. 2020. Wing geometric morphometrics of workers and drones and single nucleotide polymorphisms provide similar genetic structure in the Iberian honey bee (Apis mellifera iberiensis). Insects 11 (2): 89. DOI :10.3390/insects11020089.
Kandemir I, Özkan A, Fuchs S. 2011. Reevaluation of honeybee (Apis mellifera) microtaxonomy: a geometric morphometric approach. Apidologie (Celle) 42: 618–627. DOI: 10.1007/ s13592-011-0063-3
Klingenberg CP. 2011. MorphoJ: An integrated software package for geometric morphometrics. Mol Ecol Resour (11) : 353–357.
Leonidas C, Fani H, Maria B, Mica M, Anastasios DM. 2014. Morphological discrimination of greek honeybee populations based on geometric morphometrics analysis of wing shape. J Apic Sci 58 (1). DOI : 10.2478/JAS- 2014-000.
Marghitas AL, Paniti-Teleky O, Dezmirean D, Rodica M, Cristina B, Coroian C, Laura L, Adela M. 2008. Morphometric differences between honeybees (Apis mellifera carpatica) Populations from Transylvanian area, Scientific Papers Animal Science and Biotechnologies 41 (2): 309-315
Miguel I, Baylac M, Iriondo M, Manzano C, Garney L, Estonba A. 2011. Both geometric morphometrics and microsatellite data support the differenciation of the Apis mellifera M evolutionary branch. Apidologie (Celle) 42 (2): 150–161. DOI : 10.1051/apido/2010048.
Nawrocka A, Kandemir ?, Fuchs S, Tofilski A. 2018. Computer software for identification of honey bee subspecies and evolutionary lineages. Apidologie (Celle) 49: 172–184. DOI : 10.1007/s13592-017-0538-y. DOI : 10.1007/s13592-017-0538-y
Oleksa A, To?lski A. 2014. Wing geometric morphometrics and microsatellite analysis provide similar discrimination of Honey Bee subspecies. Apidologie (Celle) 46: 49–60. DOI : 10.1007/s13592-014-0300-7
Outomuro D, Johansson FA. 2017. Potential pitfall in studies of biological shape: Does size matter ?. J Anim Ecol 86: 1447–1457. DOI : 10.1111/1365- 2656.12732.
Pavlinov IY. 2001. Geometric morphometrics, a new analytical approach to comparision of digitized images. Information Technology in Biodiversity Research: Abstracts of the 2nd International Symposium. St. Petersburg: Russian Academy of Science, 44–64.
Prado-Silva A, Nunes LA, De Oliveira Alves RM, Carneiro PLS, Waldschmidt AM. 2016. Variation of fore wing shape in Melipona mandacaia Smith, 1863 (Hymenoptera, Meliponini) along its geographic range. J Hymenopt Res 48: 85-94. DOI : 10.3897/JHR.48.6619.
Rohlf FJ. 2001. TPS Dig 2.16 software. State University of New York at Stony Brook, NY
Rohlf FJ. 2017. tpsRelw-relative warp analysis, version 1.67. New York (NY): Stony Brook University, Stony Brook.
Rohlf FJ. 2017. Tps Utility program, Version 1.74. Ecology and Evolution and Anthropology, Stony Brook University
Ruttner F. 1988. Biogeography and Taxonomy of Honeybees. Springer, Berlin.
Sandoval Ramirez CM, Nieves Blanco EE, Gutiérrez Marin R, Jaimes Mendez DA, Rodríguez NO, Otálora-Luna F, Aldana, E. J. 2015. Morphometric analysis of the host effect on phenotypical variation of Belminus ferroae (Hemiptera: Triatominae). Psyche, 1–12. DOI : 10.1155/2015/613614
Salehi, S, Nazemi-Rafie, J. 2020. Discrimination of Iranian honeybee populations (Apis mellifera meda) from commercial subspecies of Apis mellifera L. using morphometric and genetic methods. J Asia Pac Entomol, 23, 591-598. DOI : 10.1016/j.aspen.2020.04.009
Silva F. 2015. Automated Bee Species Identification Through Wing Images. [Thesis]. University of Sao Paulo, [Brazilian].
Skandalis DA, Segre PS, Bahlman JW, Groom DJE, Welch Jr, KCW, Witt CC, McGuire JA, Dudley R, Lentink D, Altshuler DL. 2017. The biomechanical origin of extreme wing allometry in humming birds. Nat Commun 8, 1047. DOI : 10.1038/s41467-017-01223-x
Slice DE. 2002. Morpheus, For morphometric research software. Department of Biomedical Engineering, Wake Forest University School of Medicine, Winston, Salem.
Sontigun N, Sukontason KL, Zajac B, Zehner R, Sukontason K, Wannasan A, Amendt J. 2017. Wing morphometrics as a tool in species identification of forensically important blow flies of Thailand. Parasit Vectors 10:229. DOI :10.1186/s13071-017-2163-z
Sultan AA. 2015. Studying the variation of wing shape and size for Iraqi honey bee worker apis mellifera (Hymenoptera : Apidae) collected from Baghdad and Diyala provinces by using geometric morphometric of wing. Int J Curr Res 7 (1), pp.11319- 11324.
Tatsuta H, Takahashi KH, Sakamaki Y. 2018. Geometric morphometrics in entomology: Basics and applications. Entomol Sci 21 (2): 164–184. DOI : 10.1111/ens.12293. DOI : 10.1111/ens.12293
Tofilski A. 2008. Using geometric morphometrics and standard morphometry to discriminate three honeybee subspecies. Apidologie (Celle) 39: 558–563. DOI: 10.1051/apido:2008037
Townsend CR, Begon M, Harper JL. 2008. Essentials of Ecology. 3rd Edition. Wiley-Blackwell, Oxford.
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