Abstract
Islands are fascinating study systems for biogeography, allowing researchers to investigate patterns across organisms on a comparable geographical scale. They are also often important for conservation. Here, we present the first bio-inventory of the ant fauna of the Aeolian Islands, a Sicilian volcanic archipelago formed within the last million years. We documented a total of 40 species, including one first record for Italy (Lasius casevitzi). Mitochondrial DNA barcodes were obtained for all 40 taxa sampled on the islands, 13 of which were studied genetically for the first time. Mitochondrial DNA sequences of island specimens were compared with those of conspecific samples from other Aeolian Islands, Sicily and mainland Italy. Standardized photographical documentation of all sequenced specimens is provided. All but one currently recognized species (97.5%) were recovered as monophyletic. Genetic divergence within species ranged up to 12.4% in Pheidole pallidula, although most species had much lower levels of intraspecific divergence. At the scale of the Aeolian Islands, intraspecific genetic divergence varied significantly between subfamilies, with species of the subfamily Myrmicinae showing higher intraspecific divergences than the Formicinae. Comparison of specimens from the Aeolian Islands with conspecific ones from the putative source populations (Sicily and mainland Italy) suggested that the island of Panarea has the genetically most derived myrmeco-fauna among the seven focal Islands. Overall, DNA barcoding is a useful-albeit not perfect-method for classifying poorly studied groups of organisms and ants in particular.
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All data generated or analysed during this study are included in this published article and its supplementary information files and accessible via the BOLD Taxonomy Browser (project AEANT).
References
Agosti, D., & Collingwood, C. A. (1987). A provisional list of the Balkan ants (Hym. Formicidae) with a key to the worker caste. II. Key to the worker caste, including the European species without the Iberian. Mitteilungen der Schweizerischen Entomologischen Gesellschaft, 60, 261–293.
Allegrucci, G., Ketmaier, V., Russo, C. D., Rampini, M., Sbordoni, V., & Cobolli, M. (2017). Molecular phylogeography of Troglophilus cave crickets (Orthoptera, Rhaphidophoridae): a combination of vicariance and dispersal drove diversification in the East Mediterranean region. Journal of Zoological Systematics and Evolutionary Research, 55(4), 310–325. https://doi.org/10.1111/jzs.12172.
AntWeb. (2020). Version 8.31. California Academy of Science, online at https://www.antweb.org. Accessed 28 May 2020.
Baroni Urbani, C. (1964). Catalogo delle specie di Formicidae in Italia. Memorie della Società entomologica italiana, 50, 1–289.
Boer, P. (2013). Revision of the European ants of the Aphaenogaster testaceopilosa-group (Hymenoptera: Formicidae). Tijdschrift voor entomologie, 156(1), 57–93. https://doi.org/10.1163/22119434-00002022.
Buschinger, A. (2009). Social parasitism among ants: a review (Hymenoptera: Formicidae). Myrmecological News, 12(3), 219–235.
Chao, A. (1987). Estimating the population size for capture-recapture data with unequal catchability. Biometrics, 43(4), 783–791.
Clement, M., Posada, D., & Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9(10), 1657–1659. https://doi.org/10.1046/j.1365-294x.2000.01020.x.
Csösz, S., & Schulz, A. (2010). A taxonomic review of the Palaearctic Tetramorium ferox species-complex (Hymenoptera, Formicidae). Zootaxa, 2401, 1–29. https://doi.org/10.11646/zootaxa.2401.1.1.
Csösz, & Seifert, B. (2003). Ponera testacea Emery, 1895 stat n.–a sister species of P. coarctata (Latreille, 1802) (Hymenoptera, Formicidae). Acta Zoologica Academiae Scientiarum Hungaricae, 49(3), 201–214.
Dapporto, L., & Dennis, R. L. H. (2008). Island size is not the only consideration. Ranking priorities for the conservation of butterflies on Italian offshore islands. In T. R. New (Ed.), Insect conservation and islands (pp. 43–55). Dordrecht: Springer Netherlands. https://doi.org/10.1007/978-1-4020-8782-0_4.
Dapporto, L., & Dennis, R. L. H. (2009). Conservation biogeography of large Mediterranean islands. Butterfly impoverishment, conservation priorities and inferences for an ecologica “island paradigm.”. Ecography, 32(1), 169–179. https://doi.org/10.1111/j.1600-0587.2008.05600.x.
Dapporto, L., Cini, A., Vodă, R., Dincă, V., Wiemers, M., Menchetti, M., et al. (2019). Integrating three comprehensive data sets shows that mitochondrial DNA variation is linked to species traits and paleogeographic events in European butterflies. Molecular Ecology Resources, 19(6), 1623–1636.
Darwin, C. (1859). On the origin of species by means of natural selection. London: John Murray.
Dincă, V., Lee, K. M., Vila, R., & Mutanen, M. (2019). The conundrum of species delimitation: a genomic perspective on a mitogenetically super-variable butterfly. Proceedings of the Royal Society B, 286(1911), 20191311. https://doi.org/10.1098/rspb.2019.1311.
Economo, E. P., Narula, N., Friedman, N. R., Weiser, M. D., & Guénard, B. (2018). Macroecology and macroevolution of the latitudinal diversity gradient in ants. Nature Communications, 9(1), 1778. https://doi.org/10.1038/s41467-018-04218-4.
Emerson, B. C. (2003). Genes, geology and biodiversity: faunal and floral diversity on the island of Gran Canaria. Animal Biodiversity and Conservation, 26(1), 9–20.
Fattorini, S. (2011). Influence of island geography, age and landscape on species composition in different animal groups. Journal of Biogeography, 38(7), 1318–1329.
Fattorini, S., Borges, P. A. V., Dapporto, L., & Strona, G. (2017). What can the parameters of the species–area relationship (SAR) tell us? Insights from Mediterranean islands. Journal of Biogeography, 44(5), 1018–1028. https://doi.org/10.1111/jbi.12874.
Folmer, O., Black, M., Hoeh, W., Lutz, R., & Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3(5), 294–299.
Galkowski, C., Aubert, C., & Blatrix, R. (2019) Aphaenogaster ichnusa Santschi, 1925, bona species, and Redescription of Aphaenogaster subterranea (Latreille, 1798) (Hymenoptera, Formicidae). Sociobiology, 66(3), 420.
Gippoliti, S., & Amori, G. (2006). Ancient introductions of mammals in the Mediterranean Basin and their implications for conservation. Mammal Review, 36(1), 37–48. https://doi.org/10.1111/j.1365-2907.2006.00081.x.
Hajibabaei, M., Janzen, D. H., Burns, J. M., Hallwachs, W., & Hebert, P. D. N. (2006). DNA barcodes distinguish species of tropical Lepidoptera. Proceedings of the National Academy of Sciences, 103(4), 968–971. https://doi.org/10.1073/pnas.0510466103.
Hebert, P. D., Cywinska, A., Ball, S. L., & deWaard, J. R. (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London, Series B: Biological Sciences, 270(1512), 313–321. https://doi.org/10.1098/rspb.2002.2218.
Hebert, P. D., Hollingsworth, P. M., & Hajibabaei, M. (2016). From writing to reading the encyclopedia of life. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 371(1702), 20150321. https://doi.org/10.1098/rstb.2015.0321.
Hinojosa, J. C., Koubínová, D., Szenteczki, M., Pitteloud, C., Dincă, V., Alvarez, N., & Vila, R. (2019). A mirage of cryptic species: genomics uncover striking mito-nuclear discordance in the butterfly Thymelicus sylvestris. Molecular Ecology, 28, 3857–3868. https://doi.org/10.1111/mec.15153.
Hosoishi, S., & Ogata, K. (2019). Cryptic diversity in the widespread Asian ant Crematogaster rothneyi (Hymenoptera: Formicidae) inferred from morphological and genetic evidence. Zoological Studies, 58, 11. https://doi.org/10.6620/ZS.2019.58-11.
Hundsdoerfer, A. K., Lee, K. M., Kitching, I. J., & Mutanen, M. (2019). Genome-wide SNP data reveal an overestimation of species diversity in a group of hawkmoths. Genome Biology and Evolution, 11(8), 2136–2150. https://doi.org/10.1093/gbe/evz113.
Jansen, G., Savolainen, R., & Vepsäläinen, K. (2009). DNA barcoding as a heuristic tool for classifying undescribed Nearctic Myrmica ants (Hymenoptera: Formicidae). Zoologica Scripta, 38(5), 527–536. https://doi.org/10.1111/j.1463-6409.2009.00386.x.
Jucker, C., Rigato, F., & Regalin, R. (2008). Exotic ant records from Italy (Hymenoptera, Formicidae). Bollettino di Zoologia agraria e Bachicoltura, 40(1), 99–107.
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P., & Drummond, A. (2012). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28(12), 1647–1649. https://doi.org/10.1093/bioinformatics/bts199.
Ketmaier, V., & Caccone, A. (2013). Twenty years of molecular biogeography in the West Mediterranean islands of Corsica and Sardinia: lessons learnt and future prospects. In M. Silva-Opps (Ed.), Current Progress in Biological Research (pp. 71–93). Rijeka, Croatia: InTech. https://doi.org/10.5772/55458.
Kutter, H. (1927). Ein myrmekologischer Streifzug durch Sizilien. Folia myrmecologica et termitologica, 1(7), 94–104.
Lebas, C., Galkowski, C., Blatrix, R., & Wegnez, P. (2016). In D. et Niestlé (Ed.), Fourmis d’Europe Occidentale. Le Premier Guide Complet d’Europe. La Rochelle: Delachaux et Niestlé.
Lo Cascio, P. (2017). Luoghi e natura di Sicilia 1. Le Isole Eolie. (Edizioni Danaus.). Palermo.
Lo Cascio, P., Cecchi, B., Abazzi, P., & Arnone, M. (2006). A contribution to the knowledge of the Coleoptera of the Aeolian archipelago (S Tyrrhenian) (Insecta, Coleoptera). Naturalista siciliano, 30(2), 91–116.
Lo Cascio, P., & Navarra, E. (2003). Guida naturalistica alle Isole Eolie. La vita in un arcipelago vulcanico. Palermo: L’Epos.
MacArthur, R. H., Wilson, E. O. (1967) The Theory of Island Biogeography (REV-revised.). Princeton University press. http://www.jstor.org/stable/j.ctt19cc1t2
Mangiafico, S. (2019). rcompanion: functions to support extension education program evaluation. https://CRAN.R-project.org/package=rcompanion
Médail, F., & Quézel, P. (1999). Biodiversity hotspots in the Mediterranean Basin: setting global conservation priorities. Conservation Biology, 13(6), 1510–1513. https://doi.org/10.1046/j.1523-1739.1999.98467.x.
Mei, M. (1998). Lasius (Cautolasius) myrmidon n. sp.: a new hypogaeic ant from Greece (Hymenoptera Formicidae). Bollettino della Società entomologica italiana, 130(2), 177–182.
Myers, N., Mittermeier, R. A., Mittermeier, C. G., de Fonseca, G. A. B., & Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature, 403(6772), 853. https://doi.org/10.1038/35002501.
Nguyen, L.-T., Schmidt, H. A., von Haeseler, A., & Minh, B. Q. (2015). IQ-TREE: a fast and effective stochastic algorithm for estimating miximum-likelihood phylogenies. Molecular Biology and Evolution, 32(1), 268–274. https://doi.org/10.1093/molbev/msu300.
Oksanen J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., et al. (2019). Vegan: community ecology package. https://CRAN.R-project.org/package=vegan
van den Hoek Ostende, L. W., van der Geer, A. A. E. H., & Wijngaarden, C. L. (2017). Why are there no giants at the dwarves feet? Insular micromammals in the eastern Mediterranean. Quaternary International, 445, 269–278. https://doi.org/10.1016/j.quaint.2016.05.007.
Papadopoulou, A., Anastasiou, I., Keskin, B., & Vogler, A. P. (2009). Comparative phylogeography of tenebrionid beetles in the Aegean archipelago: the effect of dispersal ability and habitat preference. Molecular Ecology, 18(11), 2503–2517. https://doi.org/10.1111/j.1365-294X.2009.04207.x.
Paradis, E., Claude, J., & Strimmer, K. (2004). APE: analyses of phylogenetics and evolution in R language. Bioinformatics, 20(2), 289–290. https://doi.org/10.1093/bioinformatics/btg412.
Paulay, G. (1994). Biodiversity on oceanic islands: its origin and extinction. American Zoology, 34, 134–144. https://doi.org/10.1093/icb/34.1.134.
Pretto, F., Celesti-Grapow, L., Carli, E., Brundu, G., & Blasi, C. (2012). Determinants of non-native plant species richness and composition across small Mediterranean islands. Biological Invasions, 14(12), 2559–2572. https://doi.org/10.1007/s10530-012-0252-7.
R Core Team. (2018). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing https://www.R-project.org/.
Ratnasingham, S., & Hebert, P. D. (2007). bold: the barcode of life data system (http://www.barcodinglife.org). Molecular Ecology Notes, 7(3), 355–364. https://doi.org/10.1111/j.1471-8286.2007.01678.x.
Rosa, R. D., Guillou, H., Mazzuoli, R., & Ventura, G. (2003). New unspiked K–Ar ages of volcanic rocks of the central and western sector of the Aeolian Islands: reconstruction of the volcanic stages. Journal of Volcanology and Geothermal Research, 120(3), 161–178. https://doi.org/10.1016/S0377-0273(02)00369-4.
Salata, S., & Borowiec, L. (2015). A taxonomic revision of the genus Oxyopomyrmex André, 1881 (Hymenoptera: Formicidae). Zootaxa, 4025, 1–66. https://doi.org/10.11646/zootaxa.4025.1.1.
Sanetra, M., Güsten, R., & Schulz, A. (1999). On the taxonomy and distribution of Italian Tetramorium species and their social parasites. Memorie della Societa Entomologica Italiana, 77, 317–357.
dos Santos, A. M., Cabezas, M. P., Tavares, A. I., Xavier, R., & Branco, M. (2016). tcsBU: a tool to extend TCS network layout and visualization. Bioinformatics, 32(4), 627–628. https://doi.org/10.1093/bioinformatics/btv636.
Santschi, F. (1934). Fourmis d’une Croisière. Bullettin et Annales de la Société entomologique de Belgique, 74, 275–282.
Scalercio, S., Cini, A., Menchetti, M., Vodă, R., Bonelli, S., Bordoni, A., ... & Dapporto, L. (2020). How long is 3 km for a butterfly? Ecological constraints and functional traits explain high mitochondrial genetic diversity between Sicily and the Italian Peninsula. Journal of Animal Ecology. https://doi.org/10.1111/1365-2656.13196.
Schär, S., Talavera, G., Espadaler, X., Rana, J. D., Andersen Andersen, A., Cover, S. P., & Vila, R. (2018). Do Holarctic ant species exist? Trans-Beringian dispersal and homoplasy in the Formicidae. Journal of Biogeography, 45(8), 1917–1928. https://doi.org/10.1111/jbi.13380.
Schifani, E., & Alicata, A. (2018). Exploring the myrmecofauna of Sicily: thirty-two new ant species recorded, including six new to Italy and many new aliens (Hymenoptera, Formicidae). Polish Journal of Entomology, 87(4), 323–348. https://doi.org/10.2478/pjen-2018-0023.
Scupola, A. (2019). The Strumigenys membranifera (Emery, 1869) in Salento (Apulia) and updating its occurrence in Italy (Hymenoptera Formicidae). Bolletino del Museo Civico di Storia Naturale di Verona, 43, 25–27.
Seifert, B. (2016). Inconvenient hyperdiversity–the traditional concept of “Pheidole pallidula” includes four cryptic species (Hymenoptera: Formicidae). Soil Organisms, 88(1), 1–17. https://doi.org/10.5281/zenodo.270253.
Seifert, B., & Galkowski, C. (2016). The Westpalaearctic Lasius paralienus complex (Hymenoptera: Formicidae) contains three species. Zootaxa, 4132(1), 44–58. https://doi.org/10.11646/zootaxa.4132.1.4.
Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H., & Flook, P. (1994). Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America, 87(6), 651–701. https://doi.org/10.1093/aesa/87.6.651.
Song, H., Buhay, J. E., Whiting, M. F., & Crandall, K. A. (2008). Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proceedings of the National Academy of Sciences, 105(36), 13486–13491. https://doi.org/10.1073/pnas.0803076105.
Steiner, F. M., Csösz, S., Markó, B., Gamisch, A., Rinnhofer, L., Folterbauer, C., et al. (2018). Turning one into five: integrative taxonomy uncovers complex evolution of cryptic species in the harvester ant Messor “structor”. Molecular Phylogenetics and Evolution, 127, 387–404. https://doi.org/10.1016/j.ympev.2018.04.005.
Talavera, G., Espadaler, X., & Vila, R. (2015). Discovered just before extinction? The first endemic ant from the Balearic Islands (Lasius balearicus sp. nov.) is endangered by climate change. Journal of Biogeography, 42(3), 589–601. https://doi.org/10.1111/jbi.12438.
Toews, D. P., & Brelsford, A. (2012). The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology, 21(16), 3907–3930. https://doi.org/10.1111/j.1365-294X.2012.05664.x.
Virgilio, M., Backeljau, T., Nevado, B., & De Meyer, M. (2010). Comparative performances of DNA barcoding across insect orders. BMC Bioinformatics, 11(1), 206. https://doi.org/10.1186/1471-2105-11-206.
Vodă, R., Dapporto, L., Dincă, V., & Vila, R. (2015). Cryptic matters: overlooked species generate most butterfly beta-diversity. Ecography, 38(4), 405–409. https://doi.org/10.1111/ecog.00762.
Vodă, R., Dapporto, L., Dincă, V., Shreeve, T. G., Khaldi, M., Barech, G., et al. (2016). Historical and contemporary factors generate unique butterfly communities on islands. Scientific Reports, 6(1), 28828. https://doi.org/10.1038/srep28828.
Wagner, H. C., Arthofer, W., Seifert, B., Muster, C., Steiner, F. M., & Schlick-Steiner, B. C. (2017). Light at the end of the tunnel: integrative taxonomy delimits cryptic species in the Tetramorium caespitum complex (Hymenoptera: Formicidae). Myrmecological News, 25, 95–129. https://doi.org/10.25849/myrmecol.news_025:095.
Wallace, A. R. (1869). The Malay Archipelago: the land of the orang-utan, and the bird of paradise. A narrative of travel, with studies of man and nature, (Vol. 2). London: Macmillan and Co.
Ward, P. S., Brady, S. G., Fisher, B. L., & Schultz, T. R. (2015). The evolution of myrmicine ants: phylogeny and biogeography of a hyperdiverse ant clade (Hymenoptera: Formicidae). Systematic Entomology, 40(1), 61–81. https://doi.org/10.1111/syen.12090.
Warren, B. H., Simberloff, D., Ricklefs, R. E., Aguilée, R., Condamine, F. L., Gravel, D., Morlon, H., Mouquet, N., Rosindell, J., Casquet, J., Conti, E., Cornuault, J., Fernández-Palacios, J. M., Hengl, T., Norder, S. J., Rijsdijk, K. F., Sanmartín, I., Strasberg, D., Triantis, K. A., Valente, L. M., Whittaker, R. J., Gillespie, R. G., Emerson, B. C., & Thébaud, C. (2015). Islands as model systems in ecology and evolution: prospects fifty years after MacArthur-Wilson. Ecology Letters, 18(2), 200–217. https://doi.org/10.1111/ele.12398.
Whittaker, R. J. (1998). Island biogeography: ecology, evolution and conservation. Oxford: Oxford University Press.
Whittaker, R. J., Fernández-Palacios, J. M., Matthews, T. J., Borregaard, M. K., & Triantis, K. A. (2017). Island biogeography: taking the long view of nature’s laboratories. Science, 357(6354), eaam8326. https://doi.org/10.1126/science.aam8326.
Wielstra, B., & Arntzen, J. (2014). Exploring the effect of assymmetric mitoichondrial DNA introgression on estimating niche divergence in morphologically cryptic species. PLoS One, 9(4), e95504. https://doi.org/10.1371/journal.pone.0095504.
Xiao, J.-H., Wang, N.-X., Murphy, R. W., Cook, J., Jia, L.-Y., & Huang, D.-W. (2012). Wolbachia infection and dramatic intraspecific mitochondrial DNA divergence in a fig wasp. Evolution, 66(6), 1907–1916. https://doi.org/10.1111/j.1558-5646.2011.01561.x.
Acknowledgments
We are grateful to Christophe Galkowski for contributing with a sample of Lasius casevitzi and the collectors of some specimens used in this study, Vincenzo Gentile, Antonio Scupola, Emiliano Mori, Mirko Galuppi and Agostino Cantavenera. We also thank all participants of the Butterfly Week 2016 for making it an unforgettable event.
Funding
S. Schär was supported by the Swiss National Science Foundation (SNSF) via the Early Post-doc.Mobility grant P2SKP3_161677 and R. Vila was funded by project CGL2016- 76322-P (AEI/FEDER, UE).
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Schär, S., Menchetti, M., Schifani, E. et al. Integrative biodiversity inventory of ants from a Sicilian archipelago reveals high diversity on young volcanic islands (Hymenoptera: Formicidae). Org Divers Evol 20, 405–416 (2020). https://doi.org/10.1007/s13127-020-00442-3
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DOI: https://doi.org/10.1007/s13127-020-00442-3