Are there autochthonous Ferrissia (Mollusca Planorbidae) in thePalaearctic Molecular evidence of a widespread North Americaninvasion of the Old World

L VECCHIONI F MARRONE M ARCULEO amp V ARIZZA

Dipartimento di Scienze e Tecnologie Biologiche Chimiche e Farmaceutiche Universitagrave degli Studi di Palermo Palermo Italy

(Received 18 April 2017 accepted 27 June 2017)

AbstractIn the last few decades findings of freshwater limpets belonging to the genus Ferrissia have been frequent and widely distributedthroughout the Palaearctic and beyond The widespread presence of a Nearctic alien taxon was proved but no consensus wasachieved about the possible existence of autochthonous Ferrissia taxa in the area an occurrence which would be supported bythe presence of gastropod fossils attributed to the genus throughout Eurasia and North Africa In order to test the hypothesis of apossible persistence of autochthonous Ferrissia taxa in the Palaearctic to the present day all the published data on the geneticdiversity of Ferrissia populations occurring in the area were reviewed expanding also the currently available dataset throughdedicated sampling surveys in Italy Malta and Spain Here based on currently published and novel large ribosomal subunit 16SrRNA (16S) and cytochrome oxidase sub-unit 1 (COI) sequences the presence of the allochthonous Ferrissia californica in thewhole Palaearctic was confirmed Conversely no evidence supporting the presence of autochthonous Ferrissia taxa wasobtained Ferrissia californica proved to be a highly invasive taxon (in spite of its extremely low genetic diversity) throughoutthe invaded regions which is possibly related to the speciesrsquo ability of asexual reproduction Finally the need to investigate thepossible impact exerted by F californica on the autochthonous Palaearctic biota is briefly stressed

Keywords Biological invasions cryptic invasions Ferrissia californica genetic paradox of invasions

Introduction

Fossil records of the planorbid genus Ferrissia Walker1903 are known to occur throughout the Palaearcticregion with the genus being recorded from theMiddle Miocene of Hungary Austria southernGermany and Switzerland (Schlickum 1976 Koacutekay2006 Harzhauser et al 2012 2014b) from Pliocenedeposits of France (Wautier 1974) and from theEarly and Middle Pleistocene of Israel (Mienis ampAshkenazi 2011 Mienis amp Rittner 2013) In additionthere is doubtful fossil evidence of the presence ofFerrissia sp from interglacial Pleistocene andHolocene deposits in the Netherlands (Meijer 1987Van Der Velde 1991) and Egypt (Bernasconi ampStanley 1994) Oddly no evidence of the presenceof extant Ferrissia limpets was collected in the OldWorld until the 20th century when a few occurrences

of representatives of this genus were found in France(Roger amp Calas 1944) in Germany (Boettger 1949)and in Russia (reported by Son 2007) Afterwardsseveral findings occurred and the reported taxa wereidentified mostly under the binomia Ferrissia wautieri(Mirolli 1960) in Europe and F clessiniana (Jickeli1882) in Africa and the Middle East In fact noconsensus was reached on the taxonomic identity ofPalaearctic Ferrissia until molecular evidence (egWalther et al 2006bc Marrone et al 2011b) provedthat all the studied Ferrissia populations occurring inthe Palaearctic region belonged to a single allochtho-nous taxon of Nearctic origin initially reported as Ffragilis (Tryon 1863) and later as F californica(Rowell 1863) in accordance with the Principle ofPriority of the International Code of ZoologicalNomenclature (Christensen 2016)

Correspondence F Marrone Dipartimento di Scienze e Tecnologie Biologiche Chimiche e Farmaceutiche Universitagrave degli Studi di Palermo viaArchirafi18 I-90123 Palermo Italy Tel +39 09123891808 Fax +39 0916577210 Email federicomarroneunipait

The European Zoological Journal 2017 411ndash419Vol 84 No 1 httpsdoiorg1010802475026320171350759

copy 2017 The Author(s) Published by Informa UK Limited trading as Taylor amp Francis GroupThis is an Open Access article distributed under the terms of the Creative Commons Attribution License (httpcreativecommonsorglicensesby40) whichpermits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

From the beginning of the 21st century an ever-increasing body of evidence (Walther et al 2006a band c 2010 Beran amp Horsak 2007 Son 2007Semenchenko amp Laenko 2008 Spyra 2008 Cilia2009 Raposeiro et al 2011 Marrone et al 2011b2014 Tokinova 2012 Albrecht et al 2013) hasproved that the invasive North American Ferrissia cali-fornica widely invaded Europe Asia and SouthAmerica while a molecular identification of the taxaoccurring in Oceania (Greke 2011) and Africa (Brown1965 Khalloufiamp Boumaiza 2007) is to date lackingHowever based on the presence of Quaternary fossilsof Ferrissia in the Palaearctic the persistence of pre-Quaternary autochthonous Ferrissia populations in theregion cannot be ruled out

The present study aims to investigate the possiblepresence of autochthonous Ferrissia taxa currently liv-ing in the Palaearctic area through the aggregate ana-lysis of all the Palaearctic Ferrissia mtDNA sequencescurrently available in public repositories and addingnew data collected in the Central Mediterranean area

Materials and methods

Ferrissia specimens (one to four from each sampledsite) were collected during field surveys between 2008and 2012 on the Italian mainland (including LakeMaggiore the type locality of Ferrissia wautieri)Sardinia Sicily Malta and Spain (Table S1) the loca-tions of the newly studied populations and of those forwhich published sequences are available were mappedusing the QGIS software v 2182 (2016) (httpwwwqgisorg) and are reported in Figure 1

Water bodies were sampled with a 200-μm-mesh-sized hand net swept through the littoral vegetationand on the bottom of the studied water bodiesCollected samples were fixed in situ in 80 ethanoland sorted under a stereomicroscope The specimensidentified as Ferrissia sp according to Girod et al(1980) were then dipped in double-distilled water for1 hour and processed for DNA extraction using theQiagen ldquoDNeasy Animal Tissue Kitrdquo following themanufacturerrsquos instructions Some specimens weredeposited in the collection of the Museum of NaturalScience of the University of Florence (Zoology SectionldquoLa Specolardquo Italy see Table S1 for the cataloguenumbers) others are stored in the molluscan collectionof FedericoMarrone at theUniversity of Palermo (Italy)and are available for loan on requestA partial sequence of the cytochrome oxidase sub-

unit 1 (COI) gene was amplified using the universalprimer pair LCO1490 and HCO2198 (Folmer et al1994) A portion of the large ribosomal subunit 16SrRNA gene was amplified using the primer pairldquoSkisto-1rdquo and ldquoSkisto-2rdquo (see Marrone et al2011a) Composition of the polymerase chain reac-tion (PCR) mix and thermal cycles were performedaccording to Marrone et al (2013)After PCR amplification 5 μL of each PCR product

were separated by electrophoresis on a 2 agarose gelat 70 V for 1 h and visualised with a UVTransilluminator When PCR products showed aclear and single band of the correct expected lengththe whole PCR product was purified using the Exo-SAP purification kit and single-strand sequenced byMacrogen Inc (Seoul South Korea) with an ABI3130xL (Applied Biosystems) sequencer with the

Figure 1 Map of the sampling sites of Ferrissia spp for which mtDNA data are available

412 L Vecchioni et al

same primers used for PCR amplification Sequenceswere analysed and manually proofread with the DNAsequencing software Chromas v 262 (TechnelysiumPty Ltd 1998 Queensland Australia) and alignedwith ClustalX v 21 (Larkin et al 2007)

In addition in order to compare the new sequencesobtained with those available for other countries all ofthe 65 available COI and 17 16S rRNA Ferrissia sppsequences from the Palaearctic and the Neotropicalregions were downloaded from GenBank Moreoverall the available F californica (= F fragilis) sequencesfrom the Nearctic were downloaded for comparisonand eight Ferrissia rivularis (Say 1917) and twoPettancylus sp sequences were downloaded to beincluded as outgroups (see Albrecht et al 2006Walther et al 2010 further information on the down-loaded sequences is given in Table S1) The poor qual-ity of the available COI sequences of Ferrissia fromDenmark (Accession Number [AN] AY577502 erro-neously labelled asAcroloxus lacustris (Linnaeus 1758))and COI and 16S rRNA sequences of Ferrissia clessini-ana fromUganda (AN AY577509 and AY577469) didnot allow us to include them in the analyses

Analyses were conducted in two steps Firstly themolecular identification of the Palaearctic Ferrissiapopulations was performed through the reconstruc-tion of phylogenetic trees based on all the availablesequences for each mtDNA gene fragment respec-tively Afterwards the COI genetic diversityobserved in the Palaearctic and Neotropical biogeo-graphical regions where the single observed species(ie Ferrissia californica) proved to be allochthonouswere compared with that observed in the Nearcticwhere F californica finds its native range

The genetic identification of the studied specimensand the reconstruction of the phylogenetic relationshipsamong the taxa were performed with Bayesian infer-ence (BI) and maximum likelihood (ML) methods asimplemented in MrBayes v 326 (Ronquist et al2012) and PhyMl v 3 (Guindon amp Gascuel 2003)respectively As ameasure of branch support bootstrapvalues (Felsenstein 1985) were calculated with 1000replicates in the ML trees For both markers two inde-pendentMarkov ChainMonte Carlo analyses were runwith 1 million generations (temp 02 default priors)Trees and parameter values were sampled every 100generations resulting in 10000 saved trees per analysisin both analyses convergence was reached (EffectiveSample Size (ESS) above 93752 and 116186 respec-tively for COI and 16S rRNA) 2500 trees were con-servatively discarded as ldquoburn-inrdquo Nodesrsquo statisticalsupport of BI was evaluated by their posterior probabil-ities The choice of the best evolutionary model wasmade using PartitionFinder v 101 (Lanfear et al2012) according to the Akaike information criterion

(AIC Akaike 1974) For both the COI and 16SrRNA datasets BI and ML analyses were performedusing a HasegawandashKishinondashYano (HKY) model ofsequence evolution for molecular dataA haplotype network for all the available COI

sequences was constructed with the software Popart(v 17 httppopartotagoacnz) using the median-joining method (Bandelt et al 1999) converselydue to the low haplotype diversity observed for 16SrRNA no network was built based on this markerBased on the output of the phylogenetic analyses

the sampled populations were partitioned into twogroups (i) autochthonous populations (USA 36COI and three 16S rRNA sequences) (ii) allochtho-nous populations (Asia Europe and South America40 COI and 23 16S rRNA sequences)Analysis of molecular variance (AMOVA) (Excoffier

et al 1992) mismatch analysis haplotype diversity(Hd) and nucleotide diversity (π) were computed inorder to detect possible population differentiation withDnaSP v 5 (Librado amp Rozas 2009) Furthermore inorder to estimate the significance of the pairwise differ-ences in haplotype diversity between the two groupsthe functions described by Thomas et al (2002) andavailable at httpwwwuclacukmace-labresourcessoftware (ldquoTEST_h_DIFFrdquo) were used through thestatistical software ldquoRrdquo (v 321 R Core Team 2015available at httpswwwR-projectorg)

Results

Excluding the outgroups 76 COI sequences (per-centage of variable and parsimony-informative sites622 and 484 respectively) and 26 16S rRNAsequences (percentage of variable and parsimony-informative sites 063 and 0 respectively) wereanalysed overallBoth phylogenetic methods (ML and BI) showed

the presence of a well-supported clade (100 poster-ior probability pp and 84 bootstrap support bsin the Bayesian and ML analyses for the COI mar-ker and 100 pp and 85 bs for the 16S rRNAmarker see Figures 2 and 3) which includes all theautochthonous North American Ferrissia californicapopulations along with all the Ferrissia sp specimensto date investigated from the Palaearctic andNeotropical regions (Figures 2 and 3) Converselythe North America F rivularis clade is separatedfrom the F californica one by deep genetic distancesand well-supported nodes in accordance with itsstatus of bona species (Walther et al 2010)Overall 21 COI haplotypes were obtained

(Table S1) The haplotype network (Figure 4) indi-cates the existence of three main and widespreadhaplotypes and some rarer haplotypes shared by

Are there autochthonous Ferrissia (Mollusca Planorbidae) in the Palaearctic 413

one or a few individuals mostly restricted to singlecontinents Most of the haplotypes belong to orinclude at least one of the North American samplesexcepting the haplotypes H11 and H12 which were

observed solely in ldquoSouth America and Europerdquo andin ldquoAsiardquo respectivelyThe comparison of the two groups showed that both

nucleotide and haplotype diversity is higher in the

Figure 2 Bayesian phylogram (95 majority rule consensus tree) of the focal Ferrissia spp using the mitochondrial cytochrome oxidase 1(COI) dataset Ferrissia rivularis and Pettancylus sp were used as outgroups Node statistical support is reported as nodal posteriorprobabilities (Bayesian Inference of phylogeny BI) and bootstrap values (Maximum Likelihood ML) Asterisks indicate a bootstrapsupport value lower than 50 bull Novel sequences

414 L Vecchioni et al

Figure 3 Bayesian phylogram (95 majority rule consensus tree) of the focal Ferrissia spp using the mitochondrial 16S ribosomal subunit(16S rRNA) dataset Ferrissia rivularis and Pettancylus sp were used as outgroups Node statistical support is reported as nodal posteriorprobabilities (Bayesian Inference of phylogeny BI) and bootstrap values (Maximum Likelihood ML) Asterisks indicate a bootstrap supportvalue lower than 50 bull Novel sequences

Figure 4 Median-joining haplotype network based on a fragment of mtDNA cytochrome oxidase sub-unit 1 (COI) Dashes indicatesubstitution steps

Are there autochthonous Ferrissia (Mollusca Planorbidae) in the Palaearctic 415

ldquoautochthonousrdquo group than in the ldquoallochthonousrdquoone and this applies for both markers (Table I)AMOVA test results (Table II) show that the percen-tage of variation among the two geographical groups is1737 and within the groups it is 8263 with anFixation index (FST) value of 0173 and a p value of0000 The mismatch analysis showed an observednumber of pair-wise differences which differs signifi-cantly from the expected values (Sum of SquareDeviations (SSD) p value = 0011 raggednessindex = 0028 raggedness p value = 0039 Figure 5)

Discussion

In spite of the fossil evidence indicating the presence ofautochthonous Ferrissia species in the Palaearctic untilthe late Pleistocene or early Holocene the tree topol-ogies obtained using fragments of both COI and 16SrRNA mtDNA markers strongly support the molecu-lar homogeneity of all the current Eurasian (and SouthAmerican) Ferrissia populations and their conspecifi-city with F californica from North AmericaThe AMOVA results and the topology of the hap-

lotype network show the presence of a substantiallyhigher diversity within the group of autochthonous(ie Nearctic) populations than in the group of theallochthonous (ie Palaearctic and Neotropical)ones Moreover the haplotypes found in NorthAmerica are also present in South America andEurasia which host an impoverished subset of themolecular diversity scored in the Nearctic The onlyexceptions are the H11 and H12 haplotypes occur-ring in Europe Asia and South America which areto date absent from the Nearctic area However thelack of these haplotypes in North America is likely tobe ascribed to subsampling of Ferrissia californica inits native range (eg along the west coast of the USAcf Walther et al 2010) and it is likely that the H11and H12 haplotypes could be found there when ahigher sampling effort is performed This evidencesupports the allochthnous status of Ferrissia califor-nica in Eurasia and its North American originMoreover the mismatch analysis suggests that theentire population of Ferrissia californica is probablyunder recent demographic expansionThe occurrence of Ferrissia californica out of its native

range may be ascribed to the unwitting anthropochorusdispersal of this species along with the aquarium trade

Table I Nucleotide diversity (Pi) and haplotype diversity (Hd) ofthe ldquoautochthonousrdquo and ldquoallochthonousrdquo Ferrissia groups basedon the mitochondrial cytochrome oxidase 1 (COI) and 16S ribo-somal subunit (16S rRNA) gene fragments

Group (Pi) (Hd)

COIAutochthonous 0009 0941Allochthonous 0003 066916S rRNAAutochthonous 0004 0667Allochthonous 0 0

Table II AMOVA FST results based on 578-bp-long fragments ofthe mtDNA COI gene ldquoVardquo is the variance among groups ldquoVbrdquois the variance among populations within groups

Source ofVariation df

Sum ofsquares

Variancecomponents

Percentage ofvariation

Amonggroups

1 16419 0385 Va 17370

Withingroups

74 135489 1830 Vb 82630

Total 75 151908 2216

Fixation index (FST) 0173 p value 0000

Figure 5 Result of the mismatch distribution analysis based on a fragment of mtDNA cytochrome oxidase sub-unit 1 (COI) The dottedline represents the observed frequency distribution of pairwise differences the curve represents the expected ones

416 L Vecchioni et al

followedby its release by the aquarists through aquariumwaste disposal ndash eg Duggan (2010) reports the findingof F californica (as F fragilis) in the sediments of aqua-riums in New Zealand It has been verified that theaquarium trade is responsible for the establishment of alarge number of species into non-native areas (egMackie 1999 Rixon et al 2005) In addition there areseveral well-documented examples showing the globalinvasiveness of ldquoaquarium-dispersedrdquo gastropod spe-cies such as Potamopyrgus antipodarum (Gray 1843)Melanoides tuberculata (Muumlller 1774) and Haitia acuta(Draparnaud 1805) which invaded almost every fresh-water ecosystem of the world in less than two centuries(egDillon et al 2002Taylor 2003Bousset et al 2004Wethington amp Lydeard 2007 Albrecht et al 2009Naser et al 2011 Ladd amp Rogowski 2012 Collado2014 Marrone amp Naselli-Flores 2015)

Despite the low genetic diversity observed in non-native areas Ferrissia californica displays a note-worthy invasive capacity in markedly different areaswith suitable habitats and climates from the tempor-ary ponds of the Mediterranean area through riversand lakes of Northern Europe to tropical environ-ments in the Philippines and Brazil (eg Raposeiroet al 2011 Tokinova 2012 Albrecht et al 2013Marrone et al 2014 Lacerda et al 2015 and refer-ences therein) This is in line with the so-calledldquogenetic paradox of invasionsrdquo (Roman amp Darling2007 Caron et al 2014 Schrieber amp Lachmuth2017) based on the disappointments of the expecta-tion that a greater invasive capacity should be attrib-uted to higher genetic diversity In fact rather thanhinder invasion bottlenecks that occur during man-mediated introduction events might increase theinvasive capacity of the invader by depleting deleter-ious alleles so that even inbred individuals have ahigh fitness (see Estoup et al 2016) Furthermorethose taxa which have a non-gonochoric reproduc-tion mode (as in the case of Ferrissia californica) areoften advantaged during the colonisation of newhabitats because they have a higher potential fordemographic growth (and subsequent monopolisa-tion of resources) compared to those having a gono-choric reproduction (see Incagnone et al 2015 andreferences therein) Once it invaded a new regionFerrissia californica proved to be able to disperselocally using other physical andor biological vectorsGenetic diversity and life-history traits (eg repro-duction mode see above) are known to determinethe invasive potential of a species and its interactionswith other taxa and the combination of the twofactors seems to have favoured the spreading ofFerrissia californica throughout invaded continents

In conclusion we could not find support for thecurrent presence of indigenous Ferrissia species in

the Old World and it seems that the autochthonoustaxa previously occurring in the area did not survivethe Pleistocene or the early Holocene epochsHowever the possible presence of autochthonousFerrissia species in North Africa and the MiddleEast where Holocene subfossil records of Ferrissiawere found (see also Marrone et al 2014) cannotcurrently be ruled out Thus retrieving and analys-ing samples from these areas is now crucial in orderto assess the possible presence of autochthonousFerrissia in the Palaearctic and to test the possiblesynonymy of F clessiniana (which was describedfrom northern Egypt) with F californicaFurthermore taking into account the current lack

of studies focusing on the impact exerted by Ferrissiacalifornica on the autochthonous biota of invadedwater bodies future studies should ideally focus onthis issue evaluating whether where and how itmight be necessary to monitor and manage this spe-cies in order to minimise the possibility of this docu-mented ldquocryptic invasionrdquo to evolve into an ldquoevidenttrivialisationrdquo of the Palaearctic biodiversity

Acknowledgements

Some Ferrissia samples were kindly provided by GAlfonso (University of Salento Italy) M Bodon(University of Genova Italy) S Cianfanelli (Museumof Natural History University of Florence Italy) DCilia (St Paulrsquos Missionary College Rabat Malta) GManganelli (University of Siena Italy) N Riccardi(Italian National Research Council Institute ofEcosystem Study Verbania Italy) J Sala (Institute ofAquatic Ecology University of Girona Spain) and FStoch (Evolutionary Biology and Ecology UnitUniversiteacuteLibredeBruxellesBelgium)The commentsof two anonymous reviewers allowed us to improve afirst draft of the manuscript

Supplemental data

Supplemental data for this article can be accessed here

ORCIDL Vecchioni httporcidorg0000-0003-4325-9728F Marrone httporcidorg0000-0002-4730-0452M Arculeo httporcidorg0000-0001-8911-6736V Arizza httporcidorg0000-0002-8772-7143

References

Akaike H 1974 A new look at the statistical model identificationIEEE Transactions on Automatic Control 19716ndash723doi101109TAC19741100705

Are there autochthonous Ferrissia (Mollusca Planorbidae) in the Palaearctic 417

Figure 3 Bayesian phylogram (95 majority rule consensus tree) of the focal Ferrissia spp using the mitochondrial 16S ribosomal subunit(16S rRNA) dataset Ferrissia rivularis and Pettancylus sp were used as outgroups Node statistical support is reported as nodal posteriorprobabilities (Bayesian Inference of phylogeny BI) and bootstrap values (Maximum Likelihood ML) Asterisks indicate a bootstrap supportvalue lower than 50 bull Novel sequences

Figure 4 Median-joining haplotype network based on a fragment of mtDNA cytochrome oxidase sub-unit 1 (COI) Dashes indicatesubstitution steps

Are there autochthonous Ferrissia (Mollusca Planorbidae) in the Palaearctic 415

ldquoautochthonousrdquo group than in the ldquoallochthonousrdquoone and this applies for both markers (Table I)AMOVA test results (Table II) show that the percen-tage of variation among the two geographical groups is1737 and within the groups it is 8263 with anFixation index (FST) value of 0173 and a p value of0000 The mismatch analysis showed an observednumber of pair-wise differences which differs signifi-cantly from the expected values (Sum of SquareDeviations (SSD) p value = 0011 raggednessindex = 0028 raggedness p value = 0039 Figure 5)

Discussion

In spite of the fossil evidence indicating the presence ofautochthonous Ferrissia species in the Palaearctic untilthe late Pleistocene or early Holocene the tree topol-ogies obtained using fragments of both COI and 16SrRNA mtDNA markers strongly support the molecu-lar homogeneity of all the current Eurasian (and SouthAmerican) Ferrissia populations and their conspecifi-city with F californica from North AmericaThe AMOVA results and the topology of the hap-

lotype network show the presence of a substantiallyhigher diversity within the group of autochthonous(ie Nearctic) populations than in the group of theallochthonous (ie Palaearctic and Neotropical)ones Moreover the haplotypes found in NorthAmerica are also present in South America andEurasia which host an impoverished subset of themolecular diversity scored in the Nearctic The onlyexceptions are the H11 and H12 haplotypes occur-ring in Europe Asia and South America which areto date absent from the Nearctic area However thelack of these haplotypes in North America is likely tobe ascribed to subsampling of Ferrissia californica inits native range (eg along the west coast of the USAcf Walther et al 2010) and it is likely that the H11and H12 haplotypes could be found there when ahigher sampling effort is performed This evidencesupports the allochthnous status of Ferrissia califor-nica in Eurasia and its North American originMoreover the mismatch analysis suggests that theentire population of Ferrissia californica is probablyunder recent demographic expansionThe occurrence of Ferrissia californica out of its native

range may be ascribed to the unwitting anthropochorusdispersal of this species along with the aquarium trade

Table I Nucleotide diversity (Pi) and haplotype diversity (Hd) ofthe ldquoautochthonousrdquo and ldquoallochthonousrdquo Ferrissia groups basedon the mitochondrial cytochrome oxidase 1 (COI) and 16S ribo-somal subunit (16S rRNA) gene fragments

Group (Pi) (Hd)

COIAutochthonous 0009 0941Allochthonous 0003 066916S rRNAAutochthonous 0004 0667Allochthonous 0 0

Table II AMOVA FST results based on 578-bp-long fragments ofthe mtDNA COI gene ldquoVardquo is the variance among groups ldquoVbrdquois the variance among populations within groups

Source ofVariation df

Sum ofsquares

Variancecomponents

Percentage ofvariation

Amonggroups

1 16419 0385 Va 17370

Withingroups

74 135489 1830 Vb 82630

Total 75 151908 2216

Fixation index (FST) 0173 p value 0000

Figure 5 Result of the mismatch distribution analysis based on a fragment of mtDNA cytochrome oxidase sub-unit 1 (COI) The dottedline represents the observed frequency distribution of pairwise differences the curve represents the expected ones

416 L Vecchioni et al

followedby its release by the aquarists through aquariumwaste disposal ndash eg Duggan (2010) reports the findingof F californica (as F fragilis) in the sediments of aqua-riums in New Zealand It has been verified that theaquarium trade is responsible for the establishment of alarge number of species into non-native areas (egMackie 1999 Rixon et al 2005) In addition there areseveral well-documented examples showing the globalinvasiveness of ldquoaquarium-dispersedrdquo gastropod spe-cies such as Potamopyrgus antipodarum (Gray 1843)Melanoides tuberculata (Muumlller 1774) and Haitia acuta(Draparnaud 1805) which invaded almost every fresh-water ecosystem of the world in less than two centuries(egDillon et al 2002Taylor 2003Bousset et al 2004Wethington amp Lydeard 2007 Albrecht et al 2009Naser et al 2011 Ladd amp Rogowski 2012 Collado2014 Marrone amp Naselli-Flores 2015)

Despite the low genetic diversity observed in non-native areas Ferrissia californica displays a note-worthy invasive capacity in markedly different areaswith suitable habitats and climates from the tempor-ary ponds of the Mediterranean area through riversand lakes of Northern Europe to tropical environ-ments in the Philippines and Brazil (eg Raposeiroet al 2011 Tokinova 2012 Albrecht et al 2013Marrone et al 2014 Lacerda et al 2015 and refer-ences therein) This is in line with the so-calledldquogenetic paradox of invasionsrdquo (Roman amp Darling2007 Caron et al 2014 Schrieber amp Lachmuth2017) based on the disappointments of the expecta-tion that a greater invasive capacity should be attrib-uted to higher genetic diversity In fact rather thanhinder invasion bottlenecks that occur during man-mediated introduction events might increase theinvasive capacity of the invader by depleting deleter-ious alleles so that even inbred individuals have ahigh fitness (see Estoup et al 2016) Furthermorethose taxa which have a non-gonochoric reproduc-tion mode (as in the case of Ferrissia californica) areoften advantaged during the colonisation of newhabitats because they have a higher potential fordemographic growth (and subsequent monopolisa-tion of resources) compared to those having a gono-choric reproduction (see Incagnone et al 2015 andreferences therein) Once it invaded a new regionFerrissia californica proved to be able to disperselocally using other physical andor biological vectorsGenetic diversity and life-history traits (eg repro-duction mode see above) are known to determinethe invasive potential of a species and its interactionswith other taxa and the combination of the twofactors seems to have favoured the spreading ofFerrissia californica throughout invaded continents

In conclusion we could not find support for thecurrent presence of indigenous Ferrissia species in

the Old World and it seems that the autochthonoustaxa previously occurring in the area did not survivethe Pleistocene or the early Holocene epochsHowever the possible presence of autochthonousFerrissia species in North Africa and the MiddleEast where Holocene subfossil records of Ferrissiawere found (see also Marrone et al 2014) cannotcurrently be ruled out Thus retrieving and analys-ing samples from these areas is now crucial in orderto assess the possible presence of autochthonousFerrissia in the Palaearctic and to test the possiblesynonymy of F clessiniana (which was describedfrom northern Egypt) with F californicaFurthermore taking into account the current lack

of studies focusing on the impact exerted by Ferrissiacalifornica on the autochthonous biota of invadedwater bodies future studies should ideally focus onthis issue evaluating whether where and how itmight be necessary to monitor and manage this spe-cies in order to minimise the possibility of this docu-mented ldquocryptic invasionrdquo to evolve into an ldquoevidenttrivialisationrdquo of the Palaearctic biodiversity

Acknowledgements

Some Ferrissia samples were kindly provided by GAlfonso (University of Salento Italy) M Bodon(University of Genova Italy) S Cianfanelli (Museumof Natural History University of Florence Italy) DCilia (St Paulrsquos Missionary College Rabat Malta) GManganelli (University of Siena Italy) N Riccardi(Italian National Research Council Institute ofEcosystem Study Verbania Italy) J Sala (Institute ofAquatic Ecology University of Girona Spain) and FStoch (Evolutionary Biology and Ecology UnitUniversiteacuteLibredeBruxellesBelgium)The commentsof two anonymous reviewers allowed us to improve afirst draft of the manuscript

Supplemental data

Supplemental data for this article can be accessed here

ORCIDL Vecchioni httporcidorg0000-0003-4325-9728F Marrone httporcidorg0000-0002-4730-0452M Arculeo httporcidorg0000-0001-8911-6736V Arizza httporcidorg0000-0002-8772-7143

References

Akaike H 1974 A new look at the statistical model identificationIEEE Transactions on Automatic Control 19716ndash723doi101109TAC19741100705

Are there autochthonous Ferrissia (Mollusca Planorbidae) in the Palaearctic 417

ldquoautochthonousrdquo group than in the ldquoallochthonousrdquoone and this applies for both markers (Table I)AMOVA test results (Table II) show that the percen-tage of variation among the two geographical groups is1737 and within the groups it is 8263 with anFixation index (FST) value of 0173 and a p value of0000 The mismatch analysis showed an observednumber of pair-wise differences which differs signifi-cantly from the expected values (Sum of SquareDeviations (SSD) p value = 0011 raggednessindex = 0028 raggedness p value = 0039 Figure 5)

Discussion

In spite of the fossil evidence indicating the presence ofautochthonous Ferrissia species in the Palaearctic untilthe late Pleistocene or early Holocene the tree topol-ogies obtained using fragments of both COI and 16SrRNA mtDNA markers strongly support the molecu-lar homogeneity of all the current Eurasian (and SouthAmerican) Ferrissia populations and their conspecifi-city with F californica from North AmericaThe AMOVA results and the topology of the hap-

lotype network show the presence of a substantiallyhigher diversity within the group of autochthonous(ie Nearctic) populations than in the group of theallochthonous (ie Palaearctic and Neotropical)ones Moreover the haplotypes found in NorthAmerica are also present in South America andEurasia which host an impoverished subset of themolecular diversity scored in the Nearctic The onlyexceptions are the H11 and H12 haplotypes occur-ring in Europe Asia and South America which areto date absent from the Nearctic area However thelack of these haplotypes in North America is likely tobe ascribed to subsampling of Ferrissia californica inits native range (eg along the west coast of the USAcf Walther et al 2010) and it is likely that the H11and H12 haplotypes could be found there when ahigher sampling effort is performed This evidencesupports the allochthnous status of Ferrissia califor-nica in Eurasia and its North American originMoreover the mismatch analysis suggests that theentire population of Ferrissia californica is probablyunder recent demographic expansionThe occurrence of Ferrissia californica out of its native

range may be ascribed to the unwitting anthropochorusdispersal of this species along with the aquarium trade

Table I Nucleotide diversity (Pi) and haplotype diversity (Hd) ofthe ldquoautochthonousrdquo and ldquoallochthonousrdquo Ferrissia groups basedon the mitochondrial cytochrome oxidase 1 (COI) and 16S ribo-somal subunit (16S rRNA) gene fragments

Group (Pi) (Hd)

COIAutochthonous 0009 0941Allochthonous 0003 066916S rRNAAutochthonous 0004 0667Allochthonous 0 0

Table II AMOVA FST results based on 578-bp-long fragments ofthe mtDNA COI gene ldquoVardquo is the variance among groups ldquoVbrdquois the variance among populations within groups

Source ofVariation df

Sum ofsquares

Variancecomponents

Percentage ofvariation

Amonggroups

1 16419 0385 Va 17370

Withingroups

74 135489 1830 Vb 82630

Total 75 151908 2216

Fixation index (FST) 0173 p value 0000

Figure 5 Result of the mismatch distribution analysis based on a fragment of mtDNA cytochrome oxidase sub-unit 1 (COI) The dottedline represents the observed frequency distribution of pairwise differences the curve represents the expected ones

416 L Vecchioni et al

followedby its release by the aquarists through aquariumwaste disposal ndash eg Duggan (2010) reports the findingof F californica (as F fragilis) in the sediments of aqua-riums in New Zealand It has been verified that theaquarium trade is responsible for the establishment of alarge number of species into non-native areas (egMackie 1999 Rixon et al 2005) In addition there areseveral well-documented examples showing the globalinvasiveness of ldquoaquarium-dispersedrdquo gastropod spe-cies such as Potamopyrgus antipodarum (Gray 1843)Melanoides tuberculata (Muumlller 1774) and Haitia acuta(Draparnaud 1805) which invaded almost every fresh-water ecosystem of the world in less than two centuries(egDillon et al 2002Taylor 2003Bousset et al 2004Wethington amp Lydeard 2007 Albrecht et al 2009Naser et al 2011 Ladd amp Rogowski 2012 Collado2014 Marrone amp Naselli-Flores 2015)

Despite the low genetic diversity observed in non-native areas Ferrissia californica displays a note-worthy invasive capacity in markedly different areaswith suitable habitats and climates from the tempor-ary ponds of the Mediterranean area through riversand lakes of Northern Europe to tropical environ-ments in the Philippines and Brazil (eg Raposeiroet al 2011 Tokinova 2012 Albrecht et al 2013Marrone et al 2014 Lacerda et al 2015 and refer-ences therein) This is in line with the so-calledldquogenetic paradox of invasionsrdquo (Roman amp Darling2007 Caron et al 2014 Schrieber amp Lachmuth2017) based on the disappointments of the expecta-tion that a greater invasive capacity should be attrib-uted to higher genetic diversity In fact rather thanhinder invasion bottlenecks that occur during man-mediated introduction events might increase theinvasive capacity of the invader by depleting deleter-ious alleles so that even inbred individuals have ahigh fitness (see Estoup et al 2016) Furthermorethose taxa which have a non-gonochoric reproduc-tion mode (as in the case of Ferrissia californica) areoften advantaged during the colonisation of newhabitats because they have a higher potential fordemographic growth (and subsequent monopolisa-tion of resources) compared to those having a gono-choric reproduction (see Incagnone et al 2015 andreferences therein) Once it invaded a new regionFerrissia californica proved to be able to disperselocally using other physical andor biological vectorsGenetic diversity and life-history traits (eg repro-duction mode see above) are known to determinethe invasive potential of a species and its interactionswith other taxa and the combination of the twofactors seems to have favoured the spreading ofFerrissia californica throughout invaded continents

In conclusion we could not find support for thecurrent presence of indigenous Ferrissia species in

the Old World and it seems that the autochthonoustaxa previously occurring in the area did not survivethe Pleistocene or the early Holocene epochsHowever the possible presence of autochthonousFerrissia species in North Africa and the MiddleEast where Holocene subfossil records of Ferrissiawere found (see also Marrone et al 2014) cannotcurrently be ruled out Thus retrieving and analys-ing samples from these areas is now crucial in orderto assess the possible presence of autochthonousFerrissia in the Palaearctic and to test the possiblesynonymy of F clessiniana (which was describedfrom northern Egypt) with F californicaFurthermore taking into account the current lack

of studies focusing on the impact exerted by Ferrissiacalifornica on the autochthonous biota of invadedwater bodies future studies should ideally focus onthis issue evaluating whether where and how itmight be necessary to monitor and manage this spe-cies in order to minimise the possibility of this docu-mented ldquocryptic invasionrdquo to evolve into an ldquoevidenttrivialisationrdquo of the Palaearctic biodiversity

Acknowledgements

Some Ferrissia samples were kindly provided by GAlfonso (University of Salento Italy) M Bodon(University of Genova Italy) S Cianfanelli (Museumof Natural History University of Florence Italy) DCilia (St Paulrsquos Missionary College Rabat Malta) GManganelli (University of Siena Italy) N Riccardi(Italian National Research Council Institute ofEcosystem Study Verbania Italy) J Sala (Institute ofAquatic Ecology University of Girona Spain) and FStoch (Evolutionary Biology and Ecology UnitUniversiteacuteLibredeBruxellesBelgium)The commentsof two anonymous reviewers allowed us to improve afirst draft of the manuscript

Supplemental data

Supplemental data for this article can be accessed here

ORCIDL Vecchioni httporcidorg0000-0003-4325-9728F Marrone httporcidorg0000-0002-4730-0452M Arculeo httporcidorg0000-0001-8911-6736V Arizza httporcidorg0000-0002-8772-7143

References

Akaike H 1974 A new look at the statistical model identificationIEEE Transactions on Automatic Control 19716ndash723doi101109TAC19741100705

Are there autochthonous Ferrissia (Mollusca Planorbidae) in the Palaearctic 417

followedby its release by the aquarists through aquariumwaste disposal ndash eg Duggan (2010) reports the findingof F californica (as F fragilis) in the sediments of aqua-riums in New Zealand It has been verified that theaquarium trade is responsible for the establishment of alarge number of species into non-native areas (egMackie 1999 Rixon et al 2005) In addition there areseveral well-documented examples showing the globalinvasiveness of ldquoaquarium-dispersedrdquo gastropod spe-cies such as Potamopyrgus antipodarum (Gray 1843)Melanoides tuberculata (Muumlller 1774) and Haitia acuta(Draparnaud 1805) which invaded almost every fresh-water ecosystem of the world in less than two centuries(egDillon et al 2002Taylor 2003Bousset et al 2004Wethington amp Lydeard 2007 Albrecht et al 2009Naser et al 2011 Ladd amp Rogowski 2012 Collado2014 Marrone amp Naselli-Flores 2015)

Despite the low genetic diversity observed in non-native areas Ferrissia californica displays a note-worthy invasive capacity in markedly different areaswith suitable habitats and climates from the tempor-ary ponds of the Mediterranean area through riversand lakes of Northern Europe to tropical environ-ments in the Philippines and Brazil (eg Raposeiroet al 2011 Tokinova 2012 Albrecht et al 2013Marrone et al 2014 Lacerda et al 2015 and refer-ences therein) This is in line with the so-calledldquogenetic paradox of invasionsrdquo (Roman amp Darling2007 Caron et al 2014 Schrieber amp Lachmuth2017) based on the disappointments of the expecta-tion that a greater invasive capacity should be attrib-uted to higher genetic diversity In fact rather thanhinder invasion bottlenecks that occur during man-mediated introduction events might increase theinvasive capacity of the invader by depleting deleter-ious alleles so that even inbred individuals have ahigh fitness (see Estoup et al 2016) Furthermorethose taxa which have a non-gonochoric reproduc-tion mode (as in the case of Ferrissia californica) areoften advantaged during the colonisation of newhabitats because they have a higher potential fordemographic growth (and subsequent monopolisa-tion of resources) compared to those having a gono-choric reproduction (see Incagnone et al 2015 andreferences therein) Once it invaded a new regionFerrissia californica proved to be able to disperselocally using other physical andor biological vectorsGenetic diversity and life-history traits (eg repro-duction mode see above) are known to determinethe invasive potential of a species and its interactionswith other taxa and the combination of the twofactors seems to have favoured the spreading ofFerrissia californica throughout invaded continents

In conclusion we could not find support for thecurrent presence of indigenous Ferrissia species in

the Old World and it seems that the autochthonoustaxa previously occurring in the area did not survivethe Pleistocene or the early Holocene epochsHowever the possible presence of autochthonousFerrissia species in North Africa and the MiddleEast where Holocene subfossil records of Ferrissiawere found (see also Marrone et al 2014) cannotcurrently be ruled out Thus retrieving and analys-ing samples from these areas is now crucial in orderto assess the possible presence of autochthonousFerrissia in the Palaearctic and to test the possiblesynonymy of F clessiniana (which was describedfrom northern Egypt) with F californicaFurthermore taking into account the current lack

of studies focusing on the impact exerted by Ferrissiacalifornica on the autochthonous biota of invadedwater bodies future studies should ideally focus onthis issue evaluating whether where and how itmight be necessary to monitor and manage this spe-cies in order to minimise the possibility of this docu-mented ldquocryptic invasionrdquo to evolve into an ldquoevidenttrivialisationrdquo of the Palaearctic biodiversity

Acknowledgements

Some Ferrissia samples were kindly provided by GAlfonso (University of Salento Italy) M Bodon(University of Genova Italy) S Cianfanelli (Museumof Natural History University of Florence Italy) DCilia (St Paulrsquos Missionary College Rabat Malta) GManganelli (University of Siena Italy) N Riccardi(Italian National Research Council Institute ofEcosystem Study Verbania Italy) J Sala (Institute ofAquatic Ecology University of Girona Spain) and FStoch (Evolutionary Biology and Ecology UnitUniversiteacuteLibredeBruxellesBelgium)The commentsof two anonymous reviewers allowed us to improve afirst draft of the manuscript

Supplemental data

Supplemental data for this article can be accessed here

ORCIDL Vecchioni httporcidorg0000-0003-4325-9728F Marrone httporcidorg0000-0002-4730-0452M Arculeo httporcidorg0000-0001-8911-6736V Arizza httporcidorg0000-0002-8772-7143

References

Akaike H 1974 A new look at the statistical model identificationIEEE Transactions on Automatic Control 19716ndash723doi101109TAC19741100705

Are there autochthonous Ferrissia (Mollusca Planorbidae) in the Palaearctic 417

Albrecht C Foumlller K Clewing C Hauffe TWilke T 2013 Invadersversus endemics Alien gastropod species in ancient Lake OhridHydrobiologia 739163ndash174 doi101007s10750-013-1724-1

Albrecht C Kroll O Terrazas EM Wilke T 2009 Invasion ofancient Lake Titicaca by the globally invasive Physa acuta(Gastropoda Pulmonata Hygrophila) Biological Invasions111821ndash1826 doi101007s10530-008-9360-9

Albrecht C Kuhn K Streit B 2006 A molecular phylogeny ofPlanorboidea (Gastropoda Pulmonata) Insights fromenhanced taxon sampling Zoological Scripta 3627ndash39doi101111j1463-6409200600258x

Bandelt H Forster P Roumlhl A 1999 Median-joining networks forinferring intraspecific phylogenies Molecular Biology andEvolution 1637ndash48 doi101093oxfordjournalsmolbeva026036

Beran L Horsak M 2007 Distribution of the alien freshwatersnail Ferrissia fragilis (Tryon 1863) (GastropodaPlanorbidae) in the Czech Republic Aquatic Invasions 245ndash54 doi103391ai2007215

Bernasconi MP Stanley DJ 1994 Molluscan biofacies and theirenvironmental implications Nile Delta Lagoons Egypt TheJournal of Coastal Research 10440ndash465

Boettger CR 1949 Die Einschleppung einer nordamerikanischenSuumlsswasserschnecke der Gattung Ferrissia nach DeutschlandArchiv Fuumlr Molluskenkunde 78187

Bousset L Henry PY Sourrouille P Jarne P 2004 Populationbiology of the invasive freshwater snail Physa acuta approachedthrough genetic markers ecological characterization anddemography Molecular Ecology 132023ndash2036 doi101111j1365-294X200402200x

Brown DS 1965 Freshwater gastropod Mollusca from EthiopiaBulletin of British Museum Natural History Zoology 1237ndash94

Caron V Ede FJ Sunnucks P 2014 Unravelling the Paradox ofLoss of Genetic Variation during invasion Superclones mayexplain the success of a clonal invader PLoS One 9e97744doi101371journalpone0097744

Christensen CC 2016 Change of status and name for a Hawaiianfreshwater limpetAncylus sharpi Sykes 1900 is the invasive NorthAmerican Ferrissia californica (Rowell 1863) formerly known asFerrissia fragilis (Tryon 1863) (Gastropoda PlanorbidaeAncylinae) British Museum Occasional Paper 1185ndash8

Cilia DP 2009 On the presence of the alien freshwater gastropodFerrissia fragilis (Tryon 1863) (Gastropoda Planorbidae) inthe Maltese Islands (Central Mediterranean) BollettinoMalacologico 45123ndash127

Collado GA 2014 Out of New Zealand Molecular identificationof the highly invasive freshwater mollusk Potamopyrgus antipo-darum (Gray 1843) in South America Zoological Studies531ndash9 doi101186s40555-014-0070-y

Dillon RT Wethington AR Rhett JM Smith TP 2002Populations of the European freshwater pulmonate Physa acutaare not reproductively isolated from American Physa heterostro-pha or Physa integra Invertebrate Biology 121226ndash234doi101111j1744-74102002tb00062x

Duggan IC 2010 The freshwater aquarium trade as a vector forincidental invertebrate fauna Biological Invasions 123757ndash3770doi101007s10530-010-9768-x

Estoup A Ravignegrave V Hufbauer R Vitalis R Gautier M Facon B2016 Is there a genetic paradox of biological invasion AnnualReview of Ecology Evolution and Systematics 4751ndash72doi101146annurev-ecolsys-121415-032116

Excoffier L Smouse PE Quattro JM 1992 Analysis of molecularvariance inferred from metric distances among DNA haplo-types Application to human mitochondrial DNA restrictiondata Genetics 131479ndash491

Felsenstein J 1985 Confidence limits on phylogenies Anapproach using the bootstrap Evolution 39783ndash791doi101111evo198539issue-4

Folmer O Black M Hoeh W Lutz R Vrijenhoek R 1994 DNAprimers for amplification of mitochondrial cytochrome c oxi-dase subunit 1 from diverse metazoan invertebrates MolecularMarine Biology and Biotechnology 3294ndash299

Girod A Bianchi I Mariani M 1980 Guide per il riconoscimentodelle specie animali delle acque interne italiane Gasteropodi 1(Gastropoda Pulmonata Prosobranchia Neritidae ViviparidaeBithyniidae Valvatidae) Vol 7 Verona Consiglio Nazionaledelle Ricerche

Greke K 2011 First record of the genus Ferrissia Walker 1903(Gastropoda Planorbidae) from the Papuan region BiodiversityBiogeography and Nature Conservation in Wallacea and NewGuinea Vol 1 Dmitry Telnov (Editor) Riga TheEntomological Society of Latvia ISBN-13 9789984976846

Guindon S Gascuel O 2003 A simple fast and accurate algorithmto estimate large phylogenies bymaximum likelihood SystematicBiology 52696ndash704 doi10108010635150390235520

HarzhauserMNeubauer TA GrossM Binder H 2014b The earlyMiddle Miocene mollusc fauna of Lake Rein (Eastern AlpsAustria) Palaeontographica Abteilung A Palaeozoology ndash

Stratigraphy 3021ndash71 doi101127pala30220131Harzhauser M Neubauer TA Mandic O Zuschin M Ćorić S

2012 A Middle Miocene endemic freshwater mollusc assem-blage from an intramontane Alpine lake (Aflenz Basin EasternAlps Austria) Palaontologische Zeitschrift 8623ndash41doi101007s12542-011-0117-x

Incagnone G Marrone F Barone R Robba L Naselli-Flores L2015 How do freshwater organisms cross the ldquodry oceanrdquo Areview on passive dispersal and colonization processes with aspecial focus on temporary ponds Hydrobiologia 750103ndash123doi101007s10750-014-2110-3

Khalloufi N Boumaiza M 2007 Premiegravere citation et descrip-tion de quatre pulmoneacutes dulcicoles de Tunisie (MolluscaOrthogastropoda) Bulletin De La Socieacuteteacute Zoologique DeFrance 132191ndash204

Koacutekay J 2006 Nonmarine mollusc fauna from the Lower andMiddle Miocene Bakony Mts W Hungary GeologicaHungarica Series Palaeontologica 563ndash196

Lacerda LEM Richau CS Amaral CRI Silva DA Carvalho EFSantos SB 2015 Ferrissia fragilis (Tryon 1863) A freshwatersnail cryptic invader in Brazil revealed by morphological andmolecular data Aquatic Invasions 10157ndash168 doi103391ai

Ladd HLA Rogowski DL 2012 Egg predation and parasiteprevalence in the invasive freshwater snail Melanoides tubercu-lata (Muumlller 1774) in a west Texas spring system AquaticInvasions 7287ndash290 doi103391ai201272016

Lanfear R Calcott B Ho SYW Guindon S 2012 PartitionFinderCombined selection of partitioning schemes and substitutionmodels for phylogenetic analyses Molecular Biology andEvolution 291695ndash1701 doi101093molbevmss020

Larkin MA Blackshields G Brown NP Chenna R McGettigan PAMcWilliam H Valentin F Wallace IM Wilm A Lopez RThompson JD Gibson TJ Higgins DG 2007 Clustal W andClustal X version 20 Bioinformatics 232947ndash2948 doi101093bioinformaticsbtm404

Librado P Rozas J 2009 DnaSP version 5 A software for com-prehensive analysis of DNA polymorphism data Bioinformatics251451ndash1452 doi101093bioinformaticsbtp187

Mackie GL 1999 Mollusc invasions through the aquarium tradeIn Claudi R Leach JH editors Nonindigenous freshwaterorganisms vectors biology and impacts Boca Raton LewisPublishers pp 135ndash147

418 L Vecchioni et al

Marrone F Alfonso G Miserocchi D Lo Brutto S 2011a Firstrecord of Hemidiaptomus (Gigantodiaptomus) superbus (Schmeil1895) in Italy with notes on distribution and conservationstatus (Copepoda Calanoida Diaptomidae) Journal ofLimnology 70149ndash155 doi103274JL11-70-1-18

Marrone F Lo Brutto S Arculeo M 2011b Cryptic invasion inSouthern Europe The case of Ferrissia fragilis (PulmonataAncylidae) Mediterranean populations Biologia - SectionZoology 663484ndash490 doi102478s11756-011-0044-z

Marrone F Lo Brutto S Hundsdoerfer AK Arculeo M 2013Overlooked cryptic endemism in copepods Systematics andnatural history of the calanoid subgenus OccidodiaptomusBorutzky 1991 (Copepoda Calanoida Diaptomidae)Molecular Phylogenetics and Evolution 66190ndash212doi101016jympev201209016

Marrone F Naselli-Flores L 2015 A review on the animal xenodi-versity in Sicilian inland waters (Italy) Advances in Oceanographyand Limnology 65451 doi104081aiol20155451

Marrone F Naser MD Amaal GY Sacco F Arculeo M 2014First record of the North American cryptic invader Ferrissiafragilis (Tryon 1863) (Mollusca Gastropoda Planorbidae) inthe Middle East Zoology in the Middle East 6039ndash45doi101080093971402014892332

Meijer T 1987 Ferrissia wautieri fossiel in NederlandCorrespondentieblad Van De Nederlandse MalacologischeVereniging 238332ndash337

Mienis HK Ashkenazi S 2011 Lentic Basommatophora molluscsand hygrophilous land snails as indicators of habitat and cli-mate in the Early-Middle Pleistocene (078 Ma) at the site ofGesher Benot Yarsquoaqov (GBY) Israel Journal of HumanEvolution 60328ndash340 doi101016jjhevol201003009

Mienis HK Rittner O 2013 On the distribution and status of theRiver limpet Ancylus fluviatilis O F Muumlller 1774 (MolluscaGastropoda Planorbidae) in Israel MalaCo 9460ndash462

Naser MD Son MO Yasser AG 2011 Assessing the risks ofinvasions of aquatic invertebrates in the Shatt Al-Arab RiverRussian Journal Biological Invasions 2120ndash125 doi101134S2075111711020081

QGIS Development Team 2016 QGIS Geographic InformationSystem version 2182 Open Source Geospatial FoundationProject Available httpwwwqgisorg Accessed April 2017 1

R Core Team 2015 R A language and environment for statisticalcomputing version 321 Vienna Austria R Foundation forStatistical Computing Available httpswwwR-projectorgAccessed April 2017 1

Raposeiro PM Costa AC Martins AF 2011 On the presencedistribution and habitat of the alien freshwater snail Ferrissiafragilis (Tryon 1863) (Gastropoda Planorbidae) in the oceanicislands of the Azores Aquatic Invasions 6(SUPPL1)S13ndashS17doi103391ai20116S1003

Rixon CAM Duggan IC Bergeron NMN Ricciardi A MacIsaacHJ 2005 Invasion risks posed by the aquarium trade and livefish markets to the Laurentian Great Lakes Biodiversity andConservation 141365ndash1381 doi101007s10531-004-9663-9

Roger J Calas P 1944 Quelques mots sur les Ancylidae BulletinsMensuels - Socieacuteteacute LinneacuteenneDe Lyon 1331ndash32 doi103406linly194413136

Roman J Darling JA 2007 Paradox lost Genetic diversity andthe success of aquatic invasions Trends in Ecology ampEvolution 22454ndash464 doi101016jtree200707002

Ronquist F Teslenko M Van der Mark P Ayres DL Darling AHoumlhna S Larget B Liu L Suchard MA Huelsenbeck JP2012 MrBayes v 32 Efficient Bayesian phylogenetic infer-ence and model choice across a large model space SystematicBiology 61539ndash542 doi101093sysbiosys029

Schlickum WR 1976 Die in der pleistozaumlnen Gemeindekiesgrubevon Zwiefaltendorf ad Donau abgelagerte Molluskenfaunader Silvanaschichten Archiv Fuumlr Molluskenkunde 1071ndash31

Schrieber K Lachmuth S 2017 The Genetic Paradox ofInvasions revisited The potential role of inbreeding times envir-onment interactions in invasion success Biological Reviews92939ndash952 doi101111brv12263

Semenchenko V Laenko T 2008 First record of the invasiveNorth American gastropod Ferrissia fragilis (Tryon 1863)from the Pripyat River basin Belarus Aquatic Invasions380ndash82 doi103391ai20083112

Son MO 2007 North American freshwater limpet Ferrissia fragilis(Tryon 1863) (Gastropoda Planorbidae) - A cryptic invaderin the Northern Black Sea Region Aquatic Invasions 255ndash58doi103391ai2007216

Spyra A 2008 The septifer form of Ferrissia wautieri (Mirolli1960) found for the first time in Poland Mollusca 2695ndash98

Taylor DW 2003 Introduction to Physidae (GastropodaHygrophila) biogeography classification morphologyRevista De Biologiacutea Tropical 511ndash287

Thomas MG Weale ME Jones AL Richards M Smith ARedhead N Torroni A Scozzari R Gratrix F TarekegnA Wilson JF Capelli C Bradman N Goldstein DB2002 Founding mothers of Jewish communitiesGeographically separated Jewish groups were independentlyfounded by very few female ancestors The AmericanJournal of Human Genetics 701411ndash1420 doi101086340609

Tokinova RP 2012 The first finding of the North Americanfreshwater limpets Ferrissia fragilis (Tryon 1863) (MolluscaGastropoda) in the Middle Volga basin Russian Journal ofBiological Invasions 352ndash55 doi101134S2075111712010134

Van Der Velde G 1991 Population dynamics and population struc-ture ofFerrissia wautieri (Mirolli 1960) (Gastropoda Ancylidae) ina pond near Nijmegen (The Netherlands) HydrobiologicalBulletin 24141ndash144 doi101007BF02260431

Walther AC Burch JB Foighil DOacute 2010 Molecular phylogeneticrevision of the freshwater limpet genus Ferrissia (PlanorbidaeAncylinae) in North America yields two species Ferrissia(Ferrissia) rivularis and Ferrissia (Kincaidilla) fragilisMalacologia 5325ndash45 doi1040020400530102

Walther AC Lee T Burch JB Foighil DOacute 2006a Acroloxus lacustrisis not an ancylid A case of misidentification involving the crypticinvader Ferrissia fragilis (Mollusca Pulmonata Hygrophila)Molecular Phylogenetics and Evolution 39271ndash275doi101016jympev200508014

Walther AC Lee T Burch JB Foighil DOacute 2006b E PluribusUnum A phylogenetic and phylogeographic reassessment ofLaevapex (Pulmonata Ancylidae) a North American genusof freshwater limpets Molecular Phylogenetics and Evolution40501ndash516 doi101016jympev200603019

Walther AC Lee T Burch JB Oacute Foighil D 2006c Confirmationthat the North American ancylid Ferrissia fragilis (Tryon 1863)is a cryptic invader of European and East Asian freshwaterecosystems Journal of Molluscan Studies 72318ndash321doi101093molluseyl009

Wautier J 1974 Premiegraveres donneacutees sur la reacutepartition en Europede Ferrissia wautieri (Gastropoda Ancylidae) Bulletin De LaSocieacuteteacute Zoologique De France 99715ndash723

Wethington AR Lydeard C 2007 A molecular phylogeny ofPhysidae (Gastropoda Basommatophora) based on mitochon-drial DNA sequences Journal ofMolluscan Studies 73241ndash257doi101093molluseym|021

Are there autochthonous Ferrissia (Mollusca Planorbidae) in the Palaearctic 419