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Assessing Molecular Diversity in Native and Introduced Populations of Red Wood Ant Formica paralugubris

. 2022 Nov 16 ; 12 (22) : . [epub] 20221116

Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic

Document type Journal Article

The Formica rufa group comprises several ant species which are collectively referred to as "red wood ants" and play key roles in boreal forest ecosystems, where they are ecologically dominant and greatly influence habitat dynamics. Owing to their intense predatory activity, some of these species are used as biocontrol agents against several forest insect pests and for this aim in Italy, nearly 6000 ant nests were introduced from their native areas in the Alps to several Appeninic sites during the last century. In this work, we assessed and compared the genetic variability and structure of native and introduced populations of F. paralugubris, thus evaluating the extent of genetic drift that may have occurred since the time of introduction, using amplified fragment length polymorphism (AFLP) markers. PCR amplification with a fam_EcoRI-TAC/MseI-ATG primers combination produced a total of 147 scorable bands, with 17 identified as outlier loci. The genetic variation was higher in the introduced population compared to the native ones that, on the other hand, showed a higher diversity between nests. AMOVA results clearly pointed out that the overall genetic structure was dominated by among-worker variation, considering all populations, the Alpine vs. Apennine groups and the comparison among native and related introduced populations (all ranging between 77.84% and 79.84%). Genetic analyses unveiled the existence of six main different groups that do not entirely mirror their geographic subdivision, pointing towards a wide admixture between populations, but, at the same time, rapid diversification of some Apennine populations. Future studies based on high-throughput genomic methods are needed to obtain a thorough understanding of the effects of environmental pressure on the genetic structure and mating system of these populations.

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Stockan J., Robinson E., Trager J., Yao I., Seifert B. Introducing wood ants: Evolution, phylogeny, identification and distribution. In: Stockan J., Robinson E., editors. Wood Ant Ecology and Conservation (Ecology, Biodiversity and Conservation) 1st ed. Cambridge University Press; Cambridge, UK: 2016. pp. 1–36. DOI

Risch A.C., Ellis S., Wiswell H. Where and why? Wood ant population ecology. In: Stockan J., Robinson E., editors. Wood Ant Ecology and Conservation (Ecology, Biodiversity and Conservation) 1st ed. Cambridge University Press; Cambridge, UK: 2016. pp. 81–105. DOI

Punttila P., Niemelä P., Karhu K. The impact of wood ants (Hymenoptera: Formicidae) on the structure of invertebrate community on mountain birch (Betula pubescens ssp. czerepanovii) Ann. Zool. Fenn. 2004;41:429–446.

Ohashi M., Kilpeläinen J., Finér L., Risch A.C., Domisch T., Neuvonen S., Niemelä P. The effect of red wood ant (Formica rufa group) mounds on root biomass, density, and nutrient concentrations in boreal managed forests. Eur. J. For. Res. 2007;12:113–119. doi: 10.1007/s10310-006-0258-z. DOI

Di Nuzzo L., Masoni A., Frizzi F., Bianchi E., Castellani M.B., Balzani P., Benesperi R. Red wood ants shape epiphytic lichen assemblages in montane silver fir forests. iForest. 2022;15:71–76. doi: 10.3832/ifor3897-014. DOI

Frouz J., Jílková V., Sorvari J. Contribution of wood ants to nutrient cycling and ecosystem function. In: Stockan J., Robinson E., editors. Wood Ant Ecology and Conservation (Ecology, Biodiversity and Conservation) 1st ed. Cambridge University Press; Cambridge, UK: 2016. pp. 81–105. DOI

Balzani P., Masoni A., Venturi S., Frizzi F., Bambi M., Fani R., Santini G. CO2 biogeochemical investigation and microbial characterization of red wood ant mounds in a Southern Europe montane forest. Soil Biol. Biochem. 2022;166:108536. doi: 10.1016/j.soilbio.2021.108536. DOI

Mabelis A.A., Korczyńska J. Long-term impact of agriculture on the survival of wood ants of the Formica rufa group (Formicidae) J. Insect Conserv. 2016;20:621–628. doi: 10.1007/s10841-016-9893-7. DOI

Balzani P., Dekoninck W., Feldhaar H., Freitag A., Frizzi F., Frouz J., Santini G. Challenges and a call to action for protecting European red wood ants. Cons. Biol. 2022:e13959. doi: 10.1111/cobi.13959. PubMed DOI PMC

Gosswald K. Die Rote Waldameise im Dienste der Waldhygiene: Forstwirtschaftliche Bedeutung, Nutzung, Lebensweise, Zucht, Wermehrung und Schutt. Metta Kinau Verlag; Lüneburg, Germany: 1951. p. 160.

Ronchetti G., Mazzoldi P., Groppali R. Venticinque Anni di Osservazioni Sui Trapianti di Formica Lugubris Zett. Dalla Alpi Alle Foreste Demaniali Casentinesi (Italia centrale): (Hymen. Formicidae) Università di Pavia; Pavia, Italy: 1986. p. 121.

Ronchetti G., Groppali R. Quarantacinque Anni di Protezione Forestale con Formica lugubris Zett. (Hymenoptera Formicidae). L’esperienza di Monte d’Alpe (Appennino Ligure in Provincia di Pavia) Istituto di Entomologia dell’Università di Pavia; Pavia, Italy: 1995. p. 271.

Frizzi F., Masoni A., Quilghini G., Ciampelli P., Santini G. Chronicle of an impact foretold: The fate and effect of the introduced Formica paralugubris ant. Biol. Inv. 2018;20:3575–3589. doi: 10.1007/s10530-018-1797-x. DOI

Seifert B. The supercolonial European wood ant Formica paralugubris Seifert, 1996 (Hymenoptera: Formicidae) introduced to Canada and its predicted role in Nearctic forests. Myrmecol. News. 2016;22:11–20.

Masoni A., Frizzi F., Natali C., Bernasconi C., Ciofi C., Santini G. Molecular identification of imported red wood ant populations in the Campigna biogenetic nature Reserve (Foreste Casentinesi national Park, Italy) Cons. Gen. Res. 2019;11:231–236. doi: 10.1007/s12686-018-0982-7. DOI

Seifert B. Formica paralugubris nov. spec.—A sympatric sibling species of Formica lugubris from the western Alps (Insecta: Hymenoptera: Formicoidea: Formicidae) Reichenbachia. 1996;35:193–201.

Bernasconi C., Maeder A., Freitag A., Cherix D. Formica paralugubris (Hymenoptera, Formicidae) in the Italian Alps from new data and old data revisited. Myrmecol. News. 2006;8:251–256.

Cherix D. Note preliminaire sur la structure, la phenologie et le regime alimentaire d’une super-colonie de Formica lugubris Zett. Insect. Soc. 1980;27:226–236. doi: 10.1007/BF02223666. DOI

Chapuisat M., Goudet J., Keller L. Microsatellites reveal high population viscosity and limited dispersal in the ant Formica paralugubris. Evolution. 1997;51:475–482. doi: 10.1111/j.1558-5646.1997.tb02435.x. PubMed DOI

Holzer B., Meunier J., Keller L., Chapuisat M. Stay or drift? Queen acceptance in the ant Formica paralugubris. Insect. Soc. 2008;55:392–396. doi: 10.1007/s00040-008-1017-2. DOI

Cherix D. Red wood ants. Ethol. Ecol. Evol. 1991;3:165. doi: 10.1080/03949370.1991.10721936. DOI

Chapuisat M., Keller L. Extended family structure in the ant Formica paralugubris: The role of the breeding system. Behav. Ecol. Soc. 1999;46:405–412. doi: 10.1007/s002650050636. DOI

Blears M.J., De Grandis S.A., Lee H., Trevors J.T. Amplified fragment length polymorphism (AFLP): A review of the procedure and its applications. JIMB. 1998;21:99–114. doi: 10.1038/sj.jim.2900537. DOI

Bernasconi C., Pamilio P., Cherix D. Molecular markers allow sibling species identification in red wood ants (Formica rufa group) Syst. Entomol. 2010;35:243–249. doi: 10.1111/j.1365-3113.2009.00503.x. DOI

Balzani P., Vizzini S., Frizzi F., Masoni A., Lessard J.P., Bernasconi C., Santini G. Plasticity in the trophic niche of an invasive ant explains establishment success and long-term coexistence. Oikos. 2021;130:691–696. doi: 10.1111/oik.08217. DOI

Lienhard A., Schäffer S. Extracting the invisible: Obtaining high quality DNA is a challenging task in small arthropods. PeerJ. 2019;7:e6753. doi: 10.7717/peerj.6753. PubMed DOI PMC

Coppi A., Cecchi L., Mengoni A., Phustahija F., Tomović G., Selvi F. Low genetic diversity and contrasting patterns of differentiation in the two monotypic genera Halacsya and Paramoltkia (Boraginaceae) endemic to the Balkan serpentines. Flora. 2014;209:5–14. doi: 10.1016/j.flora.2013.11.002. DOI

Foll M., Fischer M.C., Heckel G., Excoffier L. Estimating population structure from AFLP amplification intensity. Mol. Ecol. 2010;19:4638–4647. doi: 10.1111/j.1365-294X.2010.04820.x. PubMed DOI

Burr T.L. Quasi-equilibrium theory for the distribution of rare alleles in a subdivided population: Justification and implications. Theor. Popul. Biol. 2000;57:297–306. doi: 10.1006/tpbi.2000.1453. PubMed DOI

Yang A.H., Dick C.W., Yao X.H., Huang H.W. Impacts of biogeographic history and marginal population genetics on species range limits: A case study of Liriodendron chinense. Sci. Rep. 2016;6:25632. doi: 10.1038/srep25632. PubMed DOI PMC

Nei M. Molecular Evolutionary Genetics. Columbia University Press; New York, NY, USA: 1987. p. 512.

Lewontin R.C. Evolutionary biology: The apportionment of human diversity. In: Dobzhansky T., Hecht M.K., Steere W.C., editors. Evolutionary Biology. Springer; New York, NY, USA: 1995. pp. 381–398. DOI

Yeh F., Yang R., Boyle T., Ye Z., Mao J. POPGEN Ver. 1.32. The User-Friendly Software for Population Genetic Analysis. University of Alberta, Molecular Biology and Biotechnology Center; Edmonton, AB, Canada: 1997.

Schneider S., Roessli D., Excer L. Arlequin: A Software for Population Genetics Data Analysis. University of Geneva, Genetics and Biometry Laboratory; Geneva, Switzerland: 2000.

Tamura K., Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 1993;10:512–526. doi: 10.1093/oxfordjournals.molbev.a040023. PubMed DOI

Kumar S., Nei M., Dudley J., Tamura K. MEGA: A biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief. Bioinform. 2008;9:299–306. doi: 10.1093/bib/bbn017. PubMed DOI PMC

Hubisz M.J., Falush D., Stephens M., Pritchard J.K. Inferring weak population structure with the assistance of sample group information. Mol. Ecol. Res. 2009;9:1322–1332. doi: 10.1111/j.1755-0998.2009.02591.x. PubMed DOI PMC

Evanno G., Regnaut S., Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Mol. Ecol. 2005;14:2611–2620. doi: 10.1111/j.1365-294X.2005.02553.x. PubMed DOI

Earl D.A., Von Holdt B.M. STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 2012;4:359–361. doi: 10.1007/s12686-011-9548-7. DOI

Menchetti M., Talavera G., Cini A., Salvati V., Dincă V., Platania L., Dapporto L. Two ways to be endemic. Alps and Apennines are different functional refugia during climatic cycles. Mol. Ecol. 2021;30:1297–1310. doi: 10.1111/mec.15795. PubMed DOI

Frizzi F., Masoni A., Santedicola M., Servini M., Simoncini N., Palmieri J., Santini G. Intraspecific relationships and nest mound shape are affected by habitat features in introduced populations of the red wood ant Formica paralugubris. Insects. 2022;13:198–204. doi: 10.3390/insects13020198. PubMed DOI PMC

Kulmuni J., Nouhaud P., Pluckrose L., Satokangas I., Dhaygude K., Butlin R.K. Instability of natural selection at candidate barrier loci underlying speciation in wood ants. Mol. Ecol. 2020;29:3988–3999. doi: 10.1111/mec.15606. PubMed DOI

Maky-Petays H., Zakharov A., Viljakainen L., Corander J., Pamilo P. Genetic changes associated to declining populations of Formica ants in fragmented forest landscape. Mol. Ecol. 2005;14:733–742. doi: 10.1111/j.1365-294X.2005.02444.x. PubMed DOI

Allendorf F.W., England P.R., Luikart G., Ritchie P.A., Ryman N. Genetic effects of harvest on wild animal populations. Trends Ecol. Evol. 2008;23:327–337. doi: 10.1016/j.tree.2008.02.008. PubMed DOI

Groppali R., Crudele G. Le formiche del gruppo Formica rufa trapiantate nel Parco nazionale delle Foreste Casentinesi, Monte Falterona e Campigna. Quad. Stud. Nat. Romagna. 2005;20:63–73.

Flanagan S.P., Jones A.G. The future of parentage analysis: From microsatellites to SNPs and beyond. Mol. Ecol. 2019;28:544–567. doi: 10.1111/mec.14988. PubMed DOI

Gzyl A., Augustynowicz E., Mosiej E., Zawadka M., Gniadek G., Nowaczek A., Slusarczyk J. Amplified fragment length polymorphism (AFLP) versus randomly amplified polymorphic DNA (RAPD) as new tools for inter-and intra-species differentiation within Bordetella. J. Med. Microbiol. 2005;54:333–346. doi: 10.1099/jmm.0.45690-0. PubMed DOI

Kulmuni J., Seifert B., Pamilo P. Segregation distortion causes large-scale differences between male and female genomes in hybrid ants. Proc. Nas. Acad. Sci. USA. 2010;107:7371–7376. doi: 10.1073/pnas.0912409107. PubMed DOI PMC

Schluns E.A., Neumann P., Schluns H., Hepburn H.R., Moritz R.F.A. Nestmate recognition and genetic variability among individuals from nests of the queenless ponerine ant, Streblognathus aethiopicus Smith (Hymenoptera: Formicidae) Afr. Entomol. 2006;14:95–102.

Nouhaud P., Beresford J., Kulmuni J. Assembly of a hybrid Formica aquilonia × F. polyctena ant genome from a haploid male. J. Hered. 2022;9:353–359. doi: 10.1093/jhered/esac019. PubMed DOI PMC

Portinha B., Avril A., Bernasconi C., Helanterä H., Monaghan J., Seifert B., Nouhaud P. Whole-genome analysis of multiple wood ant population pairs supports similar speciation histories, but different degrees of gene flow, across their European ranges. Mol. Ecol. 2022;31:3416–3431. doi: 10.1111/mec.16481. PubMed DOI PMC

Smith C.C., Weber J.N., Mikheyev A.S., Roces F., Bollazzi M., Kellner K., Mueller U.G. Landscape genomics of an obligate mutualism: Concordant and discordant population structures between the leafcutter ant Atta texana and its two main fungal symbiont types. Mol. Ecol. 2019;28:2831–2845. doi: 10.1111/mec.15111. PubMed DOI

Zhang Y.M., Vitone T.R., Storer C.G., Payton A.C., Dunn R.R., Hulcr J., Lucky A. From pavement to population genomics: Characterizing a long-established non-native ant in North America through citizen science and ddRADseq. Front. Ecol. Evol. 2019;7:453. doi: 10.3389/fevo.2019.00453. DOI

Jay P., Leroy M., Le Poul Y., Whibley A., Arias M., Chouteau M., Joron M. Association mapping of colour variation in a butterfly provides evidence that a supergene locks together a cluster of adaptive loci. Philos. Trans. R. Soc. B. 2022;377:20210193. doi: 10.1098/rstb.2021.0193. PubMed DOI PMC

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