Chrysomelidae; cold-adapted organism; genomic variation; phylogeography; species range; Ecology, Evolution, Behavior and Systematics; Ecology
Abstract :
[en] During the past few 100,000 years, repeated cycles of glaciation and warming episodes have radically altered the range of organisms. Numerous phylogeographic studies have investigated the impact of past climate changes on the range of temperate organisms in Europe, but we know substantially less about organisms that are adapted to colder climates. Their distributions are often currently fragmented and limited to relatively high elevations in mountainous regions and to the north of Europe. Our inferences of their range during the last glaciation appear contradictory: some studies indicate a range expansion through colonisation of the lowlands, while others suggest a range contraction because they were restricted to small refugia. In this study, we wished to identify which of these two alternative hypotheses explains best the current distribution of genetic variation in a European montane leaf beetle whose current range spans several mountains. Location: Four European mountain systems: Alps, Vosges, Massif Central, Pyrenees. Time Period: End of the Quaternary, focusing mainly on the last glaciation and the Holocene. Taxon: Gonioctena quinquepunctata [Fabricius, 1787] (Coleoptera; Chrysomelidae). Results: Modelling of the potential current and last glacial maximum species distributions suggested that climatic conditions were more favourable in the lowlands during the last glaciation, opening the possibility that this leaf beetle has colonised them at the time. Characterising genomic variation across its current range using RAD-seq data and comparing alternative hypotheses about its evolution with coalescence models in a composite likelihood framework contradicted this hypothesis; however: these analyses inferred instead that the species was associated with a much smaller population size during the last glaciation, suggesting that its range was then restricted to the mountains' outskirts. Main Conclusions: Comparing these results to those of other studies of European cold-adapted species, we argue that phylogeographic evidence points towards a similar glacial contraction of the range of many similar organisms.
Disciplines :
Zoology
Author, co-author :
Kastally, Chedly ✱; Department of Forest Sciences, University of Helsinki, Finland ; Viikki Plant Sciences Center, University of Helsinki, Finland
Sorel, Maeva ✱; Evolutionary Biology and Ecology, Université Libre de Bruxelles (ULB), Belgium
This work was supported by a Fonds d'Encouragement \u00E0 la Recherche (FER) grant from the Universit\u00E9 libre de Bruxelles and by a grant from the Belgian Fonds de la Recherche Scientifique (F.R.S.\u2010FNRS; CDR J.0075.18) to P.M. M.S. was supported by a PhD fellowship from FRS\u2010FNRS, while C.K. was supported by a postdoctoral fellowship from the Research Council of Finland (funding decision no. 348922). Computational resources were provided by the Consortium des Equipements de Calcul Intensif (CECI), funded by F.R.S.\u2010FNRS (Grant 2.5020.11) and the Walloon Region, and by CSC\u2014IT Center for Science, Finland. To comply with French legislation regarding the Nagoya protocol on access to genetic resources, a declaration has been filed with the French authorities (NOR: TREL2103218S / 449). No permits were required for sampling.This work was supported by Fonds De La Recherche Scientifique\u2014FNRS, CDR J.0075.18. Funding:
Adde, A., P.-L. Rey, F. Fopp, et al. 2023. “Too Many Candidates: Embedded Covariate Selection Procedure for Species Distribution Modelling With the Covsel R Package.” Ecological Informatics 75: 102080.
Akaike, H. 1974. “A New Look at the Statistical Model Identification.” IEEE Transactions on Automatic Control 19: 716–723.
Alexander, D. H., J. Novembre, and K. Lange. 2009. “Fast Model-Based Estimation of Ancestry in Unrelated Individuals.” Genome Research 19: 1655–1664.
Alsos, I. G., T. Alm, S. Normand, and C. Brochmann. 2009. “Past and Future Range Shifts and Loss of Diversity in Dwarf Willow (Salix Herbacea L.) Inferred From Genetics, Fossils and Modelling.” Global Ecology and Biogeography 18: 223–239.
Araújo, M. B., and M. New. 2007. “Ensemble Forecasting of Species Distributions.” Trends in Ecology & Evolution 22: 42–47.
Avise, J. 2000. Phylogeography. The History and Formation of Species. Harvard University Press.
Baird, N. A., P. D. Etter, T. S. Atwood, et al. 2008. “Rapid SNP Discovery and Genetic Mapping Using Sequenced RAD Markers.” PLoS One 3: e3376.
Benke, M., M. Brändle, C. Albrecht, and T. Wilke. 2009. “Pleistocene Phylogeography and Phylogenetic Concordance in Cold-Adapted Spring Snails (Bythinella spp.).” Molecular Ecology 18: 890–903.
Birks, H. H. 2008. “The Late-Quaternary History of Arctic and Alpine Plants.” Plant Ecology and Diversity 1: 135–146.
Bisconti, R., D. Canestrelli, P. Colangelo, and G. Nascetti. 2011. “Multiple Lines of Evidence for Demographic and Range Expansion of a Temperate Species (Hyla sarda) During the Last Glaciation.” Molecular Ecology 20: 5313–5327.
Borer, M., N. Alvarez, S. Buerki, N. Margraf, M. Rahier, and R. E. Naisbitt. 2010. “The Phylogeography of an Alpine Leaf Beetle: Divergence Within Oreina Elongata Spans Several Ice Ages.” Molecular Phylogenetics and Evolution 57: 703–709.
Carstens, B., A. R. Lemmon, and E. Moriarty Lemmon. 2012. “The Promises and Pitfalls of Next-Generation Sequencing Data in Phylogeography.” Systematic Biology 61: 713–715.
Chevalier, M., O. Broennimann, J. Cornuault, and A. Guisan. 2021. “Data Integration Methods to Account for Spatial Niche Truncation Effects in Regional Projections of Species Distribution.” Ecological Applications 31: e02427.
Collart, F., A. Hotermans, O. Broennimann, and A. Guisan. 2024. “ESM: Ensemble of Small Models. R Package Version 0.5.” https://github.com/ModInB/ESM.
Daccordi, M., N. Lavarini, and S. Ruffo. 1991. Considerazioni faunistiche e biogeografiche sulle Gonioctena italiane (Coleoptera Chrysomelidae), pp. 93–101, In Atti XVI Congresso Nazionale Italiano di Entomologia, Bari.
Dalén, L., E. Fuglei, P. Herteinsson, et al. 2005. “Population History and Genetic Structure of a Circumpolar Species: The Arctic Fox.” Biological Journal of the Linnean Society 84: 79–89.
Dalén, L., V. Nyström, C. Valdiosera, et al. 2007. “Ancient DNA Reveals Lack of Postglacial Habitat Tracking in the Arctic Fox.” Proceedings of the National Academy of Sciences of the United States of America 104: 6726–6729.
Dellicour, S., S. Fearnley, A. Lombal, et al. 2014. “Inferring the Past and Present Connectivity Across the Range of a North American Leaf Beetle: Combining Ecological Niche Modeling and a Geographically Explicit Model of Coalescence.” Evolution 68: 2371–2385.
Dormann, C. F., J. Elith, S. Bacher, et al. 2013. “Collinearity: A Review of Methods to Deal With It and a Simulation Study Evaluating Their Performance.” Ecography 36: 27–46.
Eidesen, P. B., D. Ehrich, V. Bakkestuen, et al. 2013. “Genetic Roadmap of the Arctic: Plant Dispersal Highways, Traffic Barriers and Capitals of Diversity.” New Phytologist 200: 898–910.
Emerson, K. J., C. R. Merz, J. M. Catchen, et al. 2010. “Resolving Postglacial Phylogeography Using High-Throughput Sequencing.” Proceedings of the National Academy of Sciences of the United States of America 107: 16196–16200.
Espíndola, A., L. Pellissier, L. Maiorano, W. Hordijk, A. Guisan, and N. Alvarez. 2012. “Predicting Present and Future Intra-Specific Genetic Structure Through Niche Hindcasting Across 24 Millennia.” Ecology Letters 15: 649–657.
Excoffier, L., I. Dupanloup, E. Huerta-Sánchez, V. C. Sousa, and M. Foll. 2013. “Robust Demographic Inference From Genomic and SNP Data.” PLoS Genetics 9: e1003905.
Excoffier, L., and H. E. L. Lischer. 2010. “Arlequin Suite ver 3.5: A New Series of Programs to Perform Population Genetics Analyses Under Linux and Windows.” Molecular Ecology Resources 10: 564–567.
Excoffier, L., N. Marchi, D. A. Marques, A. Gouy, and V. C. Sousa. 2021. “fastsimcoal2: Demographic Inference Under Complex Evolutionary Scenarios.” Bioinformatics 37: 4882–4885.
Garrick, R. C., I. A. S. Bonatelli, C. Hyseni, et al. 2015. “The Evolution of Phylogeographic Data Sets.” Molecular Ecology 24: 1164–1171.
Guisan, A., M. Chevalier, A. Adde, et al. 2025. “Spatially Nested Species Distribution Models (N-SDM): An Effective Tool to Overcome Niche Truncation for More Robust Inference and Projections.” Journal of Ecology in press.
Guisan, A., W. Thuiller, and N. E. Zimermann. 2017. Habitat Suitability and Distribution Models. With Applications in R. Cambridge University Press.
Gutenkunst, R. N., R. D. Hernandez, S. H. Williamson, and C. D. Bustamante. 2009. “Inferring the Joint Demographic History of Multiple Populations From Multidimensional SNP Frequency Data.” PLoS Genetics 5: e1000695.
Hewitt, G. 2000. “The Genetic Legacy of the Quaternary Ice Ages.” Nature 405: 907–913.
Hewitt, G. M. 2001. “Speciation, Hybrid Zones and Phylogeography — or Seeing Genes in Space and Time.” Molecular Ecology 10: 537–549.
Hewitt, G. M. 2004. “Genetic Consequences of Climatic Oscillations in the Quaternary.” Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 359: 183–195.
Hijmans, R. J., S. Phillips, J. Leathwick, and J. Elith. 2023. “dismo: Species Distribution Modeling_. R Package Version 1.3–14.” https://CRAN.R-project.org/package=dismo.
Hohenlohe, P. A., S. Bassham, P. D. Etter, N. Stiffler, E. A. Johnson, and W. A. Cresko. 2010. “Population Genomics of Parallel Adaptation in Threespine Stickleback Using Sequenced RAD Tags.” PLoS Genetics 6: e1000862.
Holderegger, R., and C. Thiel-Egenter. 2009. “A Discussion of Different Types of Glacial Refugia Used in Mountain Biogeography and Phylogeography.” Journal of Biogeography 36: 476–480.
Hudson, R. R. 1990. “Gene Genealogies and the Coalescent Process.” In Oxford Surveys in Evolutionary Biology, edited by D. G. Futuyma and J. Antonovics, 1–44. Oxford Univ. Press.
Johnson, J. B., and K. S. Omland. 2004. “Model Selection in Ecology and Evolution.” Trends in Ecology & Evolution 19: 101–108.
Jombart, T., and I. Ahmed. 2011. “Adegenet 1.3-1: New Tools for the Analysis of Genome-Wide SNP Data.” Bioinformatics 27: 3070–3071.
Kajtoch, L., E. Cieslak, Z. Varga, et al. 2016. “Phylogeographic Patterns of Steppe Species in Eastern Central Europe: A Review and the Implications for Conservation.” Biodiversity and Conservation 25: 2309–2339.
Karger, D. N., M. P. Nobis, S. Normand, C. H. Graham, and N. E. Zimmermann. 2023. “CHELSA-TraCE21k-High-Resolution (1 km) Downscaled Transient Temperature and Precipitation Data Since the Last Glacial Maximum.” Climate of the Past 19: 439–456.
Karger, D. N., D. Schmatz, D. Detttling, and N. E. Zimmermann. 2020. “High Resolution Monthly Precipitation and Temperature Timeseries for the Period 2006-2100.” Scientific Data 7: 248.
Kastally, C., S. Dellicour, O. J. Hardy, M. Gilbert, and P. Mardulyn. 2021. “Estimating Migration of Gonioctena Quinquepunctata (Coleoptera: Chrysomelidae) Inside a Mountain Range in a Spatially Explicit Context.” Insect Systematics and Diversity 5: 8.
Kastally, C., M. Trasoletti, and P. Mardulyn. 2019. “Limited Gene Exchange Between Two Sister Species of Leaf Beetles Within a Hybrid Zone in the Alps.” Journal of Evolutionary Biology 32: 1406–1417.
Knoll, S., M. Rowell-Rahier, P. Mardulyn, and J. M. Pasteels. 1996. “Spatial Genetic Structure of Leaf Beetle Species With Special Emphasis on Alpine Populations.” In Chrysomelidae Biology, Vol. 1: The Classification, Phylogeny and Genetics, edited by P. H. A. Cox and M. L. Ja, 379–388. SPB Academic Publishing.
Kotlik, P., V. Deffontaine, S. Mascheretti, J. Zima, J. R. Michaux, and J. B. Searle. 2006. “A Northern Glacial Refugium for Bank Voles (Clethrionomys Glareolus).” Proceedings of the National Academy of Sciences of the United States of America 103: 14860–14864.
Kropf, M., J. W. Kadereit, and H. P. Comes. 2003. “Differential Cycles of Range Contraction and Expansion in European High Mountain Plants During the Late Quaternary: Insights From Pritzelago Alpina (L.) O. Kuntze (Brassicaceae).” Molecular Ecology 12: 931–949.
Liu, X., and Y.-X. Fu. 2020. “Stairway Plot 2: Demographic History Inference With Folded SNP Frequency Spectra.” Genome Biology 21: 280.
Lohse, K., J. A. Nicholls, and G. N. Stone. 2011. “Inferring the Colonization of a Mountain Range—Refugia vs. Nunatak Survival in High Alpine Ground Beetles.” Molecular Ecology 20: 394–408.
Lukicheva, S., J.-F. Flot, and P. Mardulyn. 2021. “Genome Assembly of the Cold-Tolerant Leaf Beetle Gonioctena Quinquepunctata, an Important Resource for Studying Its Evolution and Reproductive Barriers Between Species.” Genome Biology and Evolution 13: evab134.
Lukicheva, S., and P. Mardulyn. 2021. “Whole-Genome Sequencing Reveals Asymmetric Introgression Between Two Sister Species of Cold-Resistant Leaf Beetles.” Molecular Ecology 30: 4077–4089.
Macher, J.-N., A. Rozenberg, S. U. Pauls, R. Tollrian, R. Wagner, and F. Leese. 2015. “Assessing the Phylogeographic History of the Montane Caddisfly Thremma gallicum Using Mitochondrial and Restriction-Site-Associated DNA (RAD) Markers.” Ecology and Evolution 5: 648–662.
Mardulyn, P., Y. E. Mikhailov, and J. M. Pasteels. 2009. “Testing Phylogeographic Hypotheses in a Euro-Siberian Cold-Adapted Leaf Beetle With Coalescent Simulations.” Evolution 63: 2717–2729.
Meier, J. L., V. C. Sousa, D. A. Marques, et al. 2017. “Demographic Modelling With Whole-Genome Data Reveals Parallel Origin of Similar Pundamilia Cichlid Species After Hybridization.” Molecular Ecology 26: 123–141.
Minter, M., K. K. Dasmahapatra, C. D. Thomas, et al. 2020. “Past, Current, and Potential Future Distributions of Unique Genetic Diversity in a Cold-Adapted Mountain Butterfly.” Ecology and Evolution 10: 11155–11168.
Muster, C., and T. U. Berendonk. 2006. “Divergence and Diversity: Lessons From an Arctic–Alpine Distribution (Pardosa saltuaria Group, Lycosidae).” Molecular Ecology 15: 2921–2933.
Nei, M., and W. H. Li. 1979. “Mathematical Model for Studying Genetic Variation in Terms of Restriction Endonucleases.” Proceedings of the National Academy of Sciences of the United States of America 76: 5269–5273.
Oppold, A.-M., and M. Pfenninger. 2017. “Direct Estimation of the Spontaneous Mutation Rate by Short-Term Mutation Accumulation Lines in Chironomus riparius.” Evolution Letters 1: 86–92.
Pan, D., K. Hülber, W. Willner, and G. M. Scheenweiss. 2020. “An Explicit Test of Pleistocene Survival in Peripheral Versus Nunatak Refugia in Two High Mountain Plant Species.” Molecular Ecology 29: 172–183.
Pauls, S. U., H. T. Lumbsch, and P. Haase. 2006. “Phylogeography of the Montane Caddisfly Drusus discolor: Evidence for Multiple Refugia and Periglacial Survival.” Molecular Ecology 15: 2153–2169.
Pedreschi, D., O. Garcia-Rodriguez, G. Yannic, et al. 2019. “Challenging the European Southern Refugium Hypothesis: Species-Specific Structures Versus General Patterns of Genetic Diversity and Differentiation Among Small Mammals.” Global Ecology and Biogeography 28: 262–274.
Provan, J., and K. D. Bennett. 2008. “Phylogeographic Insights Into Cryptic Glacial Refugia.” Trends in Ecology & Evolution 23: 564–571.
Quinlan, A. R., and I. M. Hall. 2010. “BEDTools: A Flexible Suite of Utilities for Comparing Genomic Features.” Bioinformatics 26: 841–842.
Quinzin, M. C., and P. Mardulyn. 2014. “Multi-Locus DNA Sequence Variation in a Complex of Four Leaf Beetle Species With Parapatric Distributions: Mitochondrial and Nuclear Introgressions Reveal Recent Hybridization.” Molecular Phylogenetics and Evolution 78: 14–24.
Quinzin, M. C., S. Normand, S. Dellicour, J.-C. Svenning, and P. Mardulyn. 2017. “Glacial Survival of Trophically Linked Boreal Species in Northern Europe.” Proceedings of the Royal Society B: Biological Sciences 284: 20162799.
Rahbek, C., M. K. Borregaard, R. K. Colwell, et al. 2019. “Humboldt's Enigma: What Causes Global Patterns of Mountain Biodiversity?” Science 365: 1108–1113.
Rank, N. E. 1992. “A Hierarchical Analysis of Genetic Differentiation in a Montane Leaf Beetle Chrysomela Aeneicollis (Coleoptera: Chrysomelidae).” Evolution 46: 1097–1111.
Rochette, N. C., A. G. Rivera-Colón, and J. M. Catchen. 2019. “Stacks 2: Analytical Methods for Paired-End Sequencing Improve RADseq-Based Population Genomics.” Molecular Ecology 28: 4737–4754.
Rousset, F. 1997. “Genetic Differentiation and Estimation of Gene Flow From F-Statistics Under Isolation by Distance.” Genetics 145: 1219–1228.
Salvi, D., P. J. Schembri, A. Sciberras, and D. J. Harris. 2014. “Evolutionary History of the Maltese Wall Lizard Podarcis Filfolensis: Insights on the ‘Expansion–Contraction’ Model of Pleistocene Biogeography.” Molecular Ecology 23: 1167–1187.
Schilthuizen, M., L. P. Santos Pimenta, Y. Lammers, et al. 2016. “Incorporation of an Invasive Plant Into a Native Insect Herbivore Food Web.” PeerJ 4: e1954.
Schmitt, T. 2007. “Molecular Biogeography of Europe: Pleistocene Cycles and Postglacial Trends.” Frontiers in Zoology 4: 11.
Schmitt, T., G. M. Hewitt, and P. Müller. 2006. “Disjunct Distributions During Glacial and Interglacial Periods in Mountain Butterflies: Erebia Epiphron as an Example.” Journal of Evolutionary Biology 19: 108–113.
Schmitt, T., C. Muster, and P. Schönswetter. 2010. “Are Disjunct Alpine and Arctic-Alpine Animal and Plant Species in the Western Palearctic Really “Relics of a Cold Past”?” In Relict Species: Phylogeography and Conservation Biology, edited by J. C. Habel and T. Assmann, 239–252. Springer-Verlag.
Schmitt, T., and Z. Varga. 2012. “Extra-Mediterranean Refugia: The Rule and Not the Exception?” Frontiers in Zoology 9: 22.
Schneeweiss, G. M., and P. Schönswetter. 2011. “A Re-Appraisal of Nunatak Survival in Arctic-Alpine Phylogeography.” Molecular Ecology 20: 190–192.
Schönswetter, P., O. Paun, A. Tribsch, and H. Niklfeld. 2003. “Out of the Alps: Colonization of Northern Europe by East Alpine Populations of the Glacier Buttercup Ranunculus glacialis L. (Ranunculaceae).” Molecular Ecology 12: 3373–3381.
Schröder, O., K. K. Cavanaugh, J. V. Schneider, et al. 2021. “Genetic Data Support Local Persistence in Multiple Glacial Refugia in the Montane Net-Winged Midge Liponeura Cinerascens Cinerascens (Diptera, Blephariceridae).” Freshwater Biology 66: 859–868.
Stewart, J. R., and L. Dalén. 2008. “Is the Glacial Refugium Concept Relevant for Northern Species? A Comment on Pruett and Winker 2005.” Climatic Change 86: 19–22.
Stewart, J. R., and A. M. Lister. 2001. “Cryptic Northern Refugia and the Origins of the Modern Biota.” Trends in Ecology & Evolution 16: 608–613.
Stewart, J. R., A. M. Lister, I. Barnes, and L. Dalén. 2010. “Refugia Revisited: Individualistic Responses of Species in Space and Time.” Proceedings of the Royal Society B: Biological Sciences 277: 661–671.
Taberlet, P., L. Fumagalli, A.-G. Wust-Saucy, and J.-F. Cossons. 1998. “Speciation, Hybrid Zones and Phylogeography — or Seeing Genes in Space and Time.” Molecular Ecology 7: 453–464.
Teacher, A. G. F., T. W. J. Garner, and R. A. Nichols. 2009. “European Phylogeography of the Common Frog (Rana temporaria): Routes of Postglacial Colonization Into the British Isles, and Evidence for an Irish Glacial Refugium.” Heredity 102: 490–496.
Theissinger, K., M. Bálint, K. A. Feldheim, et al. 2013. “Glacial Survival and Post-Glacial Recolonization of an Arctic–Alpine Freshwater Insect (Arcynopteryx Dichroa, Plecoptera, Perlodidae) in Europe.” Journal of Biogeography 40: 236–248.
Theodoridis, S., C. Randin, P. Szövényi, F. C. Boucher, T. S. Patsiou, and E. Conti. 2017. “How Do Cold-Adapted Plants Respond to Climatic Cycles? Interglacial Expansion Explains Current Distribution and Genomic Diversity in Primula farinosa L.” Systematic Biology 66: 715–736.
Thuiller, W., D. Georges, M. Gueguen, et al. 2023. “_biomod2: Ensemble Platform for Species Distribution Modeling_.” R Package Version 4: 2–4. https://CRAN.R-project.org/package=biomod2.
Toews, D. P. L., and A. Brelsford. 2012. “The Biogeography of Mitochondrial and Nuclear Discordance in Animals.” Molecular Ecology 21: 3907–3930.
Tzedakis, P. C., B. C. Emerson, and G. M. Hewitt. 2013. “Cryptic or Mystic? Glacial Tree Refugia in Northern Europe.” Trends in Ecology & Evolution 28: 696–704.
Tzedakis, P. C., I. T. Lawson, M. R. Frogley, G. M. Hewitt, and R. C. Preece. 2002. “Buffered Tree Population Changes in a Quaternary Refugium: Evolutionary Implications.” Science 297: 2044–2047.
Wachter, G. A., A. Papadopoulou, C. Muster, et al. 2016. “Glacial Refugia, Recolonization Patterns and Diversification Forces in Alpine-Endemic Megabunus Harvestmen.” Molecular Ecology 25: 2904–2919.
Weir, B. S., and C. C. Cockerham. 1984. “Estimating F-Statistics for the Analysis of Population Structure.” Evolution 38: 1358–1370.
Westergaard, K. B., I. G. Alsos, M. Popp, T. Engelskjøn, K. I. Flatberg, and C. Brochmann. 2011. “Glacial Survival May Matter After all: Nunatak Signatures in the Rare European Populations of Two West-Arctic Species.” Molecular Ecology 20: 376–393.
Kirschner, P., E. Zaveska, A. Gamish, et al. 2020. “Long-Term Isolation of European Steppe Outposts Boosts the Biome's Conservation Value.” Nature Communications 11: 1968.
Zurell, D., J. Franklin, C. König, et al. 2020. “A Standard Protocol for Reporting Species Distribution Models.” Ecography 43: 1261–1277.