Abstract
Determination of the factors influencing the population structure and adaptive tolerance to environmental pressures of the synanthropic hoverfly Eristalis arbustorum is of essential importance in understanding how pollinator populations could respond to climate change or ecosystem management. We addressed the issue of connectivity among conspecific populations sampled in Bosnia and Herzegovina. Twenty environmental factors, mitochondrial DNA sequences of the cytochrome c oxidase subunit I gene (COI mtDNA), allele frequencies at allozyme loci and wing traits (size and shape) were compared for characterization of population structure and environmental niches. Additionally, patterns of within-individual asymmetry (fluctuating asymmetry; FA) in wing size and shape within and among conspecific populations were studied. In line with the overall similarity of the environmental factors extracted for our study sites, the results of COI mtDNA diversity and STRUCTURE allozyme data provide evidence for shallow differentiation among conspecific populations. In contrast, geo-referenced Bayesian clustering methods (BAPS and GENELAND) and population-based approaches (pairwise FST values and AMOVA) indicate that the dispersal potential of E. arbustorum may be limited across the study area. Along with a significant FA in wing size and shape, a consistent level of FA regardless of urban/rural sampling origin is an indication of the great potential of E. arbustorum for local adaptation, because increased FA levels can be considered to be a way of expression of phenotypic variation and, hence, may contribute to adaptive responses in populations facing changing environments. Thus, by using a combined genetic-morphological approach, we significantly contributed to the understanding of the fine-scale genetic structure of the synanthropic generalist pollinator E. arbustorum.
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Arnfield AJ (2003) Two decades of urban climate research: a review of turbulence, exchanges of energy and water, and the urban heat island. Int J Climatol 23:1–26
Bai Y, Dong J-J, Guan D-L, **e J-Y, Xu S-Q (2016) Geographic variation in wing size and shape of the grasshopper Trilophidia annulata (Orthoptera: Oedipodidae): morphological trait variations follow an ecogeographical rule. Sci Rep 6:32680
Baldock KCR, Goddard MA, Hicks DM, Kunin WE, Mitschunas N, Osgathorpe LM, Potts SG, Robertson KM, Scott AV, Stone GN, Vaughan IP, Memmott J (2015) Where is the UK’s pollinator biodiversity? The importance of urban areas for flower-visiting insects. Proc R Soc B 282:20142849
Bates AJ, Sadler JP, Fairbrass AJ, Falk SJ, Hale JD, Matthews TJ (2011) Changing bee and hoverfly pollinator assemblages along an urban-rural gradient. PLoS ONE 6:e23459
Beasley DE, Bonisoli-Alquati A, Mousseau TA (2013) The use of fluctuating asymmetry as a measure of environmentally induced developmental instability: a meta-analysis. Ecol Indic 30:218–226
Bitner-Mathé BC, Klaczko LB (1999) Heritability, phenotypic, and genetic correlations of size and shape of Drosophila mediopunctata wings. Heredity 83:688–696
Brassel KE, Reif D (1979) A procedure to generate Thiessen polygons. Geogr Anal 325:31–36
Carter AJR, Weier TM, Houle D (2009) The effect of inbreeding on fluctuating asymmetry of wing veins in two laboratory strains of Drosophila melanogaster. Heredity 102:563–572
Carvajal TM, Hernandez LFT, Ho HT, Menard G, Cuenca MG, Orantia BMC, Estrada CR, Viacrusis KM, Amalin DM, Watanabe K (2016) Spatial analysis of wing geometry in dengue vector mosquito, Aedes aegypti (L.) (Diptera: Culicidae), populations in Metropolitan Manila, Philippines. J Vector Dis 53:127–135
Clarke GM (1995) Relationships between fluctuating asymmetry and fitness: how good is the evidence? Conserv Biol 2:146–149
Conner JK, Hartl DL (2004) A primer to ecological genetics. Sinauer Associates, Inc., Sunderland
Corander J, Marttinen P (2006) Bayesian identification of admixture events using multilocus molecular markers. Mol Ecol 15:2833–2843
Corander J, Waldmann P, Sillanpää MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 163:367–374
Corander J, Waldmann P, Marttinen P, Sillanpää MJ (2004) BAPS 2: enhanced possibilities for the analysis of genetic population structure. Bioinformatics 20:2363–2369
Corander J, Marttinen P, Sirén J, Tang J (2008) Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinform 9:539
De Buck N (1990) Bloembezoek en bestuivingsecologie van Zweefvliegen (Diptera, Syrphidae) in het bijzonder voor België. Studiedocumenten van het K.B.I.N, Brussel
Deguines N, Julliard R, de Flores M, Fontaine C (2012) The whereabouts of flower visitors: contrasting land-use preferences revealed by a country-wide survey based on citizen science. PLoS ONE 7:e4582
Dryden IL, Mardia KV (1998) Statistical shape analysis. Wiley, Chichester
Dujardin JP (2011) Modern morphometrics of medically important insects. In: Tibayrenc M (ed) Genetics and evolution of infectious disease. Elsevier, Burlington, pp 473–501
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491
Francuski L, Milankov V (2015) Assessing the spatial population structure and heterogeneity in the dronefly. J Zool 297:286–300
Francuski L, Ludoški J, Vujić A, Milankov V (2009) Wing geometric morphometric inferences on species delimitation and intraspecific divergent units in the Merodon ruficornis group (Diptera, Syrphidae) from the Balkan Peninsula. Zool Sci 26:301–308
Francuski L, Matić I, Ludoški J, Milankov V (2011) Temporal pattern of genetic and phenotypic variation of epidemiologically important species Eristalis tenax. Med Vet Entomol 25:135–147
Francuski L, Djurakic M, Ståhls G, Milankov V (2014) Landscape genetics and wing morphometrics show a lack of structuring across island and coastal populations of the drone fly in the Mediterranean. J Zool 292:156–169
Gaggiotti OE, Lange O, Rassmann K, Gliddon C (1999) A comparison of two indirect methods for estimating average levels of gene flow using microsatellite data. Mol Ecol 8:1513–1520
Gatter W, Schmid U (1990) Wanderungen der Schwebfligen (Diptera, Syrphidae) am Randecker Maar. Spixiana 15:1–100
González-Varo JP, Biesmeijer JC, Bommarco R, Potts SG, Schweiger O, Smith HG, Steffan-Dewenter I, Szentgyörgyi H, Woyciechowski M, Vilà M (2013) Combined effects of global change pressures on animal-mediated pollination. Trends Ecol Evol 28:524–530
Guillot G, Mortier F, Estoup A (2005) GENELAND: a computer package for landscape genetics. Mol Ecol Notes 5:712–715
Guillot G, Santos F, Estoup A (2008) Analysing georeferenced population genetics data with Geneland: a new algorithm to deal with null alleles and a friendly graphical user interface. Bioinformatics 24:1406–1407
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Res 41:95–98
Hall DM, Camilo GR, Tonietto RK, Ollerton J, Ahrné K, Arduser M, Ascher JS, Baldock KCR, Fowler R, Frankie G, Goulson D, Gunnarsson B, Hanley ME, Jackson JI, Langellotto G, Lowenstein D, Minor ES, Philpott SM, Potts SG, Sirohi MH, Spevak EM, Stone GN, Threlfall CG (2017) The city as a refuge for insect pollinators. Conserv Biol 31:24–29
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:3–9
Heal JR (1981) Colour patterns of Syrphidae: III. Sexual dimorphism in Eristalis arbustorum. Ecol Entomol 6:119–127
Hennig EI, Ghazoul J (2012) Pollinating animals in the urban environment. Urban Ecosyst 15:149–166
Hijmans RJ, Guarino L, Cruz M, Rojas E (2001) Computer tools for spatial analysis of plant genetic resources data: 1. DIVA-GIS. Plant Genet Resour C 127:15–19
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978
Hippa H, Nielsen TR, van Steenis J (2001) The West Palearctic species of the genus Eristalis Latreille (Diptera, Syrphidae). Norw J Entomol 48:289–327
Jones EL, Leather SR (2012) Invertebrates in urban areas: a review. Eur J Entomol 109:463–478
Juste J, López-González C, Strauss RE (2001) Analysis of asymmetries in the African fruit bats Eidolon helvum and Rousettus egyptiacus (Mammalia: Megachiroptera) from islands of the Gulf of Guinea. II. Integration and levels of multivariate fluctuating asymmetry across a geographical range. J Evol Biol 14:672–680
Klecka J, Hadrava J, Biella P, Akter A (2018) Flower visitation by hoverflies (Diptera: Syrphidae) in a temperate plant-pollinator network. PeerJ 6:e6025
Klingenberg CP (2011) MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 11:353–357
Klingenberg CP, McIntyre GS (1998) Geometric morphometrics of developmental instability: analysing patterns of fluctuating asymmetry with Procrustes methods. Evolution 52:1363–1375
Klingenberg CP, Barluenga M, Meyer A (2002) Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution 56:1909–1920
Knierim U, Van Dongen S, Forkman B, Tuyttens FAM, Spinka M, Campo JL, Weissengruber GE (2007) Fluctuating asymmetry as an animal welfare indicator—a review of methodology and validity. Physiol Behav 92:398–421
Knouft JH, Losos JB, Glor RE, Kolbe JJ (2006) Phylogenetic analysis of the evolution of the niche in lizards of the Anolis sagrei group. Ecology 87:29–38
Kölliker-Ott UM, Blows MW, Hoffmann AA (2003) Are wing size, wing shape and asymmetry related to field fitness to Trichogramma egg parasitoids? Oikos 100:563–573
Leaché AD (2011) Multi-locus estimates of population structure and migration in a fence lizard hybrid zone. PLoS ONE 6:e25827
Leary RF, Allendorf FW (1989) Fluctuating asymmetry as an indicator of stress: implications for conservation biology. Trends Ecol Evol 4:214–217
Lens L, Van Dongen S, Kark S, Matthysen E (2002a) Fluctuating asymmetry as an indicator of fitness: can we bridge the gap between studies? Biol Rev 77:27–38
Lens L, Van Dongen S, Matthysen E (2002b) Fluctuating asymmetry as an early warning system in the critically endangered Taita Thrush. Conserv Biol 16:479–487
Lucas A, Bodger O, Brosi BJ, Ford CR, Forman DW, Greig C, Hegarty M, Neyland PJ, de Vere N (2018) Generalisation and specialisation in hoverfly (Syrphidae) grassland pollen transport networks revealed by DNA metabarcoding. J Anim Ecol 87:1008–1021
Ludoški J, Lj Francuski, Vujić A, Milankov V (2008) The Cheilosia canicularis group (Diptera: Syrphidae): species delimitation and evolutionary relationships based on wing geometric morphometrics. Zootaxa 1825:40–50
Ludoški J, Djurakic M, Ståhls G, Milankov V (2012) Patterns of asymmetry in wing traits of three island and one continental population of the Merodon albifrons (Diptera, Syrphidae) species from Greece. Evol Ecol Res 14:933–950
Ludoški J, Djurakic M, Pastor B, Martínez-Sánchez AI, Rojo S, Milankov V (2014) Phenotypic variation of the housefly, Musca domestica: amounts and patterns of wing shape asymmetry in wild populations and laboratory colonies. Bull Entomol Res 104:35–47
Luxbacher AM, Knouft JH (2009) Assessing concurrent patterns of environmental niche and morphological evolution among species of horned lizards (Phrynosoma). J Evol Biol 22:1669–1678
Manel S, Schwartz M, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197
Manel S, Berthoud F, Bellemain E, Gaudeul M, Luikart G, Swenson JE, Waits LP, Taberlet P (2007) A new individual-based spatial approach for identifying genetic discontinuities in natural populations. Mol Ecol 16:2031–2043
Markow TA (1995) Evolutionary ecology and developmental instability. Annu Rev Entomol 40:105–120
Matta BP, Bitner-Mathé BC (2004) Genetic architecture of wing morphology in Drosophila simulans and an analysis of temperature effects on genetic parameter estimates. Heredity 93:330–341
McIntyre NE (2000) Ecology of urban arthropods: a review and a call to action. Ann Entomol Soc Am 93:825–835
McKinney ML (2004) Measuring floristic homogenization by non-native plants in North America. Global Ecol Biogeogr 13:47–53
Milankov V, Ludoški J, Ståhls G, Stamenković J, Vujić A (2009) High molecular and phenotypic diversity in the Merodon avidus complex (Diptera, Syrphidae): cryptic speciation in a diverse insect taxon. Zool J Linn Soc 155:819–833
Milankov V, Ludoški J, Lj Francuski, Ståhls G, Vujić A (2013) Genetic and phenotypic diversity patterns in Merodon albifrons Meigen, 1822 (Diptera, Syrphidae): evidence of intraspecific spatial and temporal structuring. Biol J Linn Soc 110:257–280
Miller MP (2005) ALLELES IN SPACE (AIS): computer software for the joint analysis of interindividual spatial and genetic information. J Hered 96:722–724
Monmonier MS (1973) Maximum-difference barriers: an alternative numerical regionalization method. Geogr Anal 5:245–261
Munstermann LE (1979) Isozymes of Aedes aegypti: Phenotypes, linkage, and use of genetic analysis of sympatric population in East Africa. PhD dissertation, University of Notre Dame
Nouvellet P, Ramirey-Sierra MJ, Domonteil E, Gourbière S (2011) Effects of genetic factors and infection status on wing morphology of Triatoma dimidiata species complex in Yucatán peninsula, Mexico. Infect Genet Evol 11:1243–1249
Oke TR (1982) The energetic basis of the urban heat island. Q J Roy Meteor Soc 108:1–24
Ottenheim MM, Volmer AD (1999) Wing length plasticity in Eristalis arbustorum (Diptera: Syrphidae). Neth J Zool 49:15–27
Ottenheim MM, Volmer AD, Holloway GJ (1996) The genetics of phenotypic plasticity in adult abdominal colour pattern of Eristalis arbustorum (Diptera: Syrphidae). Heredity 77:493–499
Ottenheim MM, Hensler A, Brakefield PM (1998) Geographic variation in plasticity in Eristalis arbustorum. Biol J Linn Soc 65:215–229
Ottenheim MM, Wertheim B, Holloway GJ, Brakefield PM (1999) Survival of colour-polymorphic Eristalis arbustorum hoverflies in semi-field conditions. Funct Ecol 13:72–77
Palmer AR, Strobeck C (1986) Fluctuating asymmetry: measurement, analysis, patterns. Annu Rev Ecol Evol S 17:391–421
Palmer AR, Strobeck C (1992) Fluctuating asymmetry as a measure of developmental stability: implications of non-normal distributions and power statistical tests. Acta Zool Fenn 191:57–72
Pasteur N, Pasteur G, Bonhomme F, Catalan J, Britton-Davidian J (1988) Practical isozyme genetics. Ellis Horwood Limited, Chichester
Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353
Powney GD, Carvell C, Edwards M, Morris RKA, Roy HE, Woodcock BA, Isaac NJB (2019) Widespread losses of pollinating insects in Britain. Nat Commun 10:1018
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
R Development Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org
Ratnieks FL, Carreck NL (2010) Ecology: clarity on honey bee collapse? Science 8:152–153
Reeve MW, Fowler K, Partridge L (2000) Increased body size confers greater fitness at lower experimental temperature in male Drosophila melanogaster. J Evol Biol 13:836–844
Rohlf FJ (2016) TpsDig, version 2.26. Department of Ecology and Evolution, State University of New York at Stony Brook. http://life.bio.sunysb.edu/morph/
Rotheray EL, Bussière LF, Moore P, Bergstrom L, Goulson D (2014) Mark recapture estimates of dispersal ability and observations on the territorial behaviour of the rare hoverfly, Hammerschmidtia ferruginea (Diptera, Syrphidae). J Insect Conserv 18:179–188
Sánchez-Bayo F, Wyckhuys KAG (2019) Worldwide decline of the entomofauna: a review of its drivers. Biol Conserv 232:8–27
Segelbacher G, Cushman SA, Epperson BK, Fortin M-J, Francois O, Hardy OJ, Holderegger R, Taberlet P, Waits LP, Manel S (2010) Applications of landscape genetics in conservation biology: concepts and challenges. Conserv Genet 11:375–385
Sekar S (2011) A meta-analysis of the traits affecting dispersal ability in butterflies: can wingspan be used as a proxy? J Anim Ecol 8:174–184
Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighing, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87:651–701
Simons AM, Johnston MO (1997) Developmental instability as a bet-hedging strategy. Oikos 80:401–406
Speight MCD, Castella E, Sarthou JP (2017) StN 2015. Syrph the net on CD, issue 10. Syrph the Net Publications. In: Speight MCD, Castella E, Sarthou JP, Vanappelghem C (eds) Syrph the Net Publications, Dublin, pp 1–291
Ståhls G, Vujić AA, Petanidou T, Cardoso P, Radenković SR, Ačanski JM, Pérez-Bañón C, Rojo S (2016) Phylogeographic patterns of Merodon hoverflies in the Eastern Mediterranean region: revealing connections and barriers. Ecol Evol 6:2226–2245
Stanley DA, Gunning D, Stout J (2003) Pollinators and pollination of oilseed rape crops (Brassica napus L.) in Ireland: ecological and economic incentives for pollinator conservation. J Insect Conserv 17:1181–1189
Stevens VM, Trochet A, Van Dyck H, Clobert J, Baguette M (2012) How is dispersal integrated in life histories: a quantitative analysis using butterflies. Ecol Lett 15:74–86
Theodorou P, Albig K, Radzeviciute R, Settele J, Schweiger O, Murray TSE, Paxton RJ (2017) The structure of flower visitor networks in relation to pollination across an agricultural to urban gradient. Funct Ecol 31:838–847
Theodorou P, Radzeviciute R, Kahnt B, Soro A, Grosse I, Paxton RJ (2018) Genome-wide single nucleotide polymorphisms can suggests adaptation to urbanization in an important pollinator, the red-tailed bumblebee (Bombus lapidaries L.). Proc R Soc B 285:20172806
Thyselius M, Nordström K (2016) Hoverfly locomotor activity is resilient to external influence and intrinsic factors. J Comp Physiol A 202:45–54
Van Dongen S (1999) Accuracy and power in fluctuating asymmetry studies: effects of sample size and number of within-subject repeats. J Evol Biol 12:547–550
Van Dongen S (2006) Fluctuating asymmetry and developmental instability in evolutionary biology: past, present and future. J Evol Biol 19:1727–1743
Van Dongen S, Lens L, Pape E, Volckaert FAM, Raeymaekers JAM (2009) Evolutionary history shapes the association between developmental instability and population-level genetic variation in three-spined sticklebacks. J Evol Biol 22:1695–1707
Vanparys V, Meerts P, Jacquemart A-L (2008) Plant-pollinator interactions: comparison between an invasive and a native congeneric species. Acta Oecol 34:361–369
Watson DF (1992) Contouring: a guide to the analysis and display of spatial data. Pergamon Press, New York
Willmore KE, Young NM, Richtsmeier JT (2007) Phenotypic variability: its components, measurement and underlying developmental processes. Evol Biol 34:99–120
Wratten SD, Bowie MH, Hickman JM, Evans AM, Sedcole JR, Tylianakis JM (2003) Field boundaries as barriers to movement of hoverflies (Diptera: Syrphidae) in cultivated land. Oecologia 134:605–611
Wright S (1951) The genetical structure of populations. Ann Eug 15:323–354
Yu H, Qiang L (2004) Foraging and pollination insects of Paeonia lactiflora. Kunchong Zhishi 41:449–454
Acknowledgements
The authors thank the reviewers for their constructive criticisms and helpful comments on earlier drafts of the manuscript. We are also grateful to Nemanja Gojkovic (University of Novi Sad) for language editing and comments on an early version on the manuscript. We thank dr Edward Petri (University of Novi Sad) for careful editing of the final manuscript for English grammar and usage. This work was supported by the Ministry of Education, Science and Technological Development of Serbia (Dynamics of gene pool, genetic and phenotypic variability of populations, determined by the environmental changes, No. OI173012).
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Francuski, L., Ludoški, J., Lukač, M. et al. Fine scale population structure of hoverfly pollinator, Eristalis arbustorum: an integrative study. J Insect Conserv 24, 49–63 (2020). https://doi.org/10.1007/s10841-019-00202-5
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DOI: https://doi.org/10.1007/s10841-019-00202-5