دورية أكاديمية

Genomic, morphological and physiological data support fast ecotypic differentiation and incipient speciation in an alpine diving beetle.

التفاصيل البيبلوغرافية
العنوان: Genomic, morphological and physiological data support fast ecotypic differentiation and incipient speciation in an alpine diving beetle.
المؤلفون: Pallarés S; Department of Zoology, University of Seville, Seville, Spain., Ortego J; Department of Ecology and Evolution, Estación Biológica de Doñana, EBD-CSIC, Seville, Spain., Carbonell JA; Department of Zoology, University of Seville, Seville, Spain., Franco-Fuentes E; Department of Zoology, University of Seville, Seville, Spain., Bilton DT; School of Biological and Marine Sciences, University of Plymouth, Plymouth, UK.; Department of Zoology, University of Johannesburg, Johannesburg, South Africa., Millán A; Department of Ecology and Hydrology, University of Murcia, Murcia, Spain., Abellán P; Department of Zoology, University of Seville, Seville, Spain.
المصدر: Molecular ecology [Mol Ecol] 2024 Sep; Vol. 33 (17), pp. e17487. Date of Electronic Publication: 2024 Aug 07.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Blackwell Scientific Publications Country of Publication: England NLM ID: 9214478 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1365-294X (Electronic) Linking ISSN: 09621083 NLM ISO Abbreviation: Mol Ecol Subsets: MEDLINE
أسماء مطبوعة: Original Publication: Oxford, UK : Blackwell Scientific Publications, c1992-
مواضيع طبية MeSH: Coleoptera*/genetics , Coleoptera*/classification , Coleoptera*/anatomy & histology , Genetic Speciation* , Phylogeny* , Genetics, Population*, Animals ; Ecotype ; Phenotype ; Spain ; Genotype ; Genetic Variation
مستخلص: An intricate interplay between evolutionary and demographic processes has frequently resulted in complex patterns of genetic and phenotypic diversity in alpine lineages, posing serious challenges to species delimitation and biodiversity conservation planning. Here we integrate genomic data, geometric morphometric analyses and thermal tolerance experiments to explore the role of Pleistocene climatic changes and adaptation to alpine environments on patterns of genomic and phenotypic variation in diving beetles from the taxonomically complex Agabus bipustulatus species group. Genetic structure and phylogenomic analyses revealed the presence of three geographically cohesive lineages, two representing trans-Palearctic and Iberian populations of the elevation-generalist A. bipustulatus and another corresponding to the strictly-alpine A. nevadensis, a narrow-range endemic taxon from the Sierra Nevada mountain range in southeastern Iberia. The best-supported model of lineage divergence, along with the existence of pervasive genetic introgression and admixture in secondary contact zones, is consistent with a scenario of population isolation and connectivity linked to Quaternary climatic oscillations. Our results suggest that A. nevadensis is an alpine ecotype of A. bipustulatus, whose genotypic, morphological and physiological differentiation likely resulted from an interplay between population isolation and local altitudinal adaptation. Remarkably, within the Iberian Peninsula, such ecotypic differentiation is unique to Sierra Nevada populations and has not been replicated in other alpine populations of A. bipustulatus. Collectively, our study supports fast ecotypic differentiation and incipient speciation processes within the study complex and points to Pleistocene glaciations and local adaptation along elevational gradients as key drivers of biodiversity generation in alpine environments.
(© 2024 The Author(s). Molecular Ecology published by John Wiley & Sons Ltd.)
References: Abellán, P., & Svenning, J. C. (2014). Refugia within refugia–patterns in endemism and genetic divergence are linked to late quaternary climate stability in the Iberian Peninsula. Biological Journal of the Linnean Society, 113, 13–28.
Adams, D. C., & Otarola‐Castillo, E. (2013). Geomorph: An r package for the collection and analysis of geometric morphometric shape data. Methods in Ecology and Evolution, 4, 393–399.
Alves, P. C., Melo‐Ferreira, J., Frieyas, H., & Boursot, P. (2008). The ubiquitous mountain hare mitochondria: Multiple introgressive hybridization in hares, genus Lepus. Philosophical Transactions of the Royal Society B: Biological Sciences, 363, 2831–2839.
Alves, V. M., Hernandez, M. I., & Lobo, J. M. (2018). Elytra absorb ultraviolet radiation but transmit infrared radiation in Neotropical Canthon species (Coleoptera, Scarabaeinae). Photochemistry and Photobiology, 94, 532–539.
Anderson, E. C., & Thompson, E. A. (2002). A model‐based method for identifying species hybrids using multilocus genetic data. Genetics, 160, 1217–1229.
Anderson, M. J., & Ter Braak, C. J. F. (2003). Permutation tests for multi‐factorial analysis of variance. Journal of Statistical Computation and Simulation, 73, 85–113.
Angus, R. B., Clery, M. J., Carter, J. C., & Wenczek, D. E. (2013). Karyotypes of some medium‐sized Dytiscidae (Agabinae and Colymbetinae) (Coleoptera). Comparative Cytogenetics, 7, 171–190.
Antonelli, A., Kissling, W. D., Flantua, S. G., Bermúdez, M. A., Mulch, A., Muellner‐Riehl, A. N., Kreft, H., Linder, H. P., Badgley, C., Fjeldså, J., Fritz, S. A., Rahbek, C., Herman, F., Hooghiemstra, H., & Hoorn, C. (2018). Geological and climatic influences on mountain biodiversity. Nature Geoscience, 11, 718–725.
Arribas, P., Velasco, J., Abellán, P., Sánchez‐Fernández, D., Andújar, C., Calosi, P., Millán, A., Ribera, I., & Bilton, D. T. (2012). Dispersal ability rather than ecological tolerance drives differences in range size between lentic and lotic water beetles (Coleoptera: Hydrophilidae). Journal of Biogeography, 39, 984–994.
Arroyo, J., Abellán, P., Arista, M., Ariza, M. J., de Castro, A., Escudero, M., Lorite, J., Martínez‐Borda, E., Mejías, J. A., Molina‐Venegas, R., Pleguezuelos, J. M., Simón‐Porcar, V., & Viruel, J. (2022). Sierra Nevada, a Mediterranean biodiversity super hotspot. In R. Zamora & M. Oliva (Eds.), The landscape of the Sierra Nevada: A unique Laboratory of Global Processes in Spain (pp. 11–30). Springer International Publishing.
Avise, J. C. (2000). Phylogeography: The history and formation of species. Harvard University Press.
Baker, A. J. (2008). Islands in the sky: The impact of Pleistocene climate cycles on biodiversity. Journal of Biology, 7, 32.
Balfour‐Browne, W. A. F. (1950). British water beetles (Vol. 2). Ray Society.
Behm, J. E., Ives, A. R., & Boughman, J. W. (2010). Breakdown in postmating isolation and the collapse of a species pair through hybridization. American Naturalist, 175, 11–26.
Bennett, K. D., & Provan, J. (2008). What do we mean by ‘refugia’? Quaternary Science Reviews, 27, 2449–2455.
Bergsten, J., Bilton, D. T., Fujisawa, T., Elliott, M., Monaghan, M. T., Balke, M., Hendrich, L., Geijer, J., Herrmann, J., Foster, G. N., Ribera, I., Nilsson, A. N., Barraclough, T. G., & Vogler, A. P. (2012). The effect of geographical scale of sampling on DNA barcoding. Systematic Biology, 61, 851–869.
Bertola, L. D., Quinn, L., Hanghøj, K., Garcia‐Erill, G., Rasmussen, M. S., Balboa, R. F., Meisner, J., Bøggild, T., Wang, X., Lin, L., Nursyifa, C., Liu, X., Li, Z., Chege, M., Moodley, Y., Brüniche‐Olsen, A., Kuja, J., Schubert, M., Agaba, M., … Heller, R. (2024). Giraffe lineages are shaped by major ancient admixture events. Current Biology, 34, 1576–1586.
Butlin, R. (1987). Speciation by reinforcement. Trends in Ecology & Evolution, 2, 8–13.
Calosi, P., Bilton, D. T., Spicer, J. I., Votier, S. C., & Atfield, A. (2010). What determines a species' geographical range? Thermal biology and latitudinal range size relationships in European diving beetles (Coleoptera: Dytiscidae). Journal of Animal Ecology, 79, 194–204.
Carbonell, J. A., Pallarés, S., Velasco, J., Millán, A., & Abellán, P. (2024). Thermal tolerance does not explain the altitudinal segregation of lowland and alpine aquatic insects. Journal of Thermal Biology, 121, 103862.
Catchen, J., Hohenlohe, P. A., Bassham, S., Amores, A., & Cresko, W. A. (2013). stacks: An analysis tool set for population genomics. Molecular Ecology, 22(11), 3124–3140.
Chen, G., & Hare, M. (2008). Cryptic ecological diversification of a planktonic estuarine copepod, Acartia tonsa. Molecular Ecology, 17, 1451–1468.
Chifman, J., & Kubatko, L. (2014). Quartet inference from SNP data under the coalescent model. Bioinformatics, 30(23), 3317–3324.
Chown, S. L., & Terblanche, J. S. (2006). Physiological diversity in insects: Ecological and evolutionary contexts. Advances in Insect Physiology, 33, 50–152.
Čiamporová‐Zaovičová, Z., & Čiampor, F. (2011). Aquatic beetles of the alpine lakes: Diversity, ecology and small‐scale population genetics. Knowledge and Management of Aquatic Ecosystems, 402, 10.
Coates, D. J., Byrne, M., & Moritz, C. (2018). Genetic diversity and conservation units: Dealing with the species‐population continuum in the age of genomics. Frontiers in Ecology and Evolution, 6, 165.
Collyer, M. L., Sekora, D. J., & Adams, D. C. (2015). A method for analysis of phenotypic change for phenotypes described by high‐dimensional data. Heredity, 115, 357–365.
Degerlund, M., Huseby, S., Zingone, A., Sarno, D., & Landfald, B. (2012). Functional diversity in cryptic species of Chaetoceros socialis Lauder (Bacillariophyceae). Journal of Plankton Research, 34, 416–431.
Drotz, M. K., Brodin, T., & Nilsson, A. N. (2010). Multiple origins of elytral reticulation modifications in the west Palearctic Agabus bipustulatus complex (Coleoptera, Dytiscidae). PLoS One, 5, e9034.
Drotz, M. K., Brodin, T., Saura, A., & Giles, B. E. (2012). Ecotype differentiation in the face of gene flow within the diving beetle Agabus bipustulatus (Linnaeus, 1767) in northern Scandinavia. PLoS One, 7, e31381.
Drotz, M. K., Saura, A., & Nilsson, A. N. (2001). The species delimitation problem applied to the Agabus bipustulatus complex (Coleoptera, Dytiscidae) in north Scandinavia. Biological Journal of the Linnean Society, 73, 11–22.
Dynesius, M., & Jansson, R. (2000). Evolutionary consequences of changes in species' geographical distributions driven by Milankovitch climate oscillations. Proceedings of the National Academy of Sciences United States of America, 97, 9115–9120.
Dynesius, M., & Jansson, R. (2014). Persistence of within‐species lineages: A neglected control of speciation rates. Evolution, 68, 923–934.
Earl, D. A., & vonHoldt, B. M. (2012). structure harvester: A website and program for visualizing structure output and implementing the Evanno method. Conservation Genetics Resources, 4(2), 359–361.
Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software v: A simulation study. Molecular Ecology, 14(8), 2611–2620.
Excoffier, L., Dupanloup, I., Huerta‐Sanchez, E., Sousa, V. C., & Foll, M. (2013). Robust demographic inference from genomic and SNP data. PLoS Genetics, 9(10), e1003905.
Excoffier, L., & Lischer, H. E. (2010). arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10(3), 564–567.
Fick, S. E., & Hijmans, R. J. (2017). WorldClim 2: New 1km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37, 4302–4315.
Flantua, S. G., Payne, D., Borregaard, M. K., Beierkuhnlein, C., Steinbauer, M. J., Dullinger, S., Essl, F., Irl, S. D. H., Kienle, D., Kreft, H., Lenzner, B., Norder, S. J., Rijsdijk, K. F., Rumpf, S. B., Weigelt, P., & Field, R. (2020). Snapshot isolation and isolation history challenge the analogy between mountains and islands used to understand endemism. Global Ecology and Biogeography, 29, 1651–1673.
Galewski, K., & Tranda, E. (1978). Fauna Słodkowodna Polski, Chrz szcze (Coleoptera), Rodziny Pływakowate (Dytiscidae), Fliskowate (Haliplidae), Mokrzelicowate (Hygrobiidae), Kretakowate (Gyrinidae) (p. 396). PWN.
García‐Vázquez, D., Bilton, D. T., Foster, G. N., & Ribera, I. (2017). Pleistocene range shifts, refugia and the origin of widespread species in western Palaearctic water beetles. Molecular Phylogenetics and Evolution, 114, 122–136.
Garrick, R. C., Benavides, E., Russello, M. A., Hyseni, C., Edwards, D. L., Gibbs, J. P., Tapia, W., Ciofi, C., & Caccone, A. (2014). Lineage fusion in Galápagos giant tortoises. Molecular Ecology, 23, 5276–5290.
Gonzalez, V. H., Oyen, K., Vitale, N., & Ospina, R. (2022). Neotropical stingless bees display a strong response in cold tolerance with changes in elevation. Conservation Physiology, 10, coac073.
Gómez, A., & Lunt, D. H. (2007). Refugia within refugia: Patterns of phylogeographic concordance in the Iberian Peninsula. In S. Weiss & N. Ferrand (Eds.), Phylogeography of southern European Refugia: Evolutionary perspectives on the origins and conservation of European biodiversity (pp. 155–188). Springer.
Gómez‐Ortiz, A., Oliva, M., Salvà‐Catarineu, M., & Salvador‐Franch, F. (2013). The environmental protection of landscapes in the high semiarid Mediterranean mountain of Sierra Nevada National Park (Spain): Historical evolution and future perspectives. Applied Geography, 42, 227–239.
Goodall, C. R. (1991). Procrustes methods in the statistical analysis of shape. Journal of the Royal Statistical Society Series B, 53, 285–339.
Gruber, B., Unmack, P. J., Berry, O. F., & Georges, A. (2018). dartR: An r package to facilitate analysis of SNP data generated from reduced representation genome sequencing. Molecular Ecology Resources, 18(3), 691–699.
Hedin, M., Carlson, D., & Coyle, F. (2015). Sky Island diversification meets the multispecies coalescent–divergence in the spruce‐fir moss spider (Microhexura montivaga, Araneae, Mygalomorphae) on the highest peaks of southern Appalachia. Molecular Ecology, 24, 3467–3484.
Hedrick, P. W. (2013). Adaptive introgression in animals: Examples and comparison to new mutation and standing variation as sources of adaptive variation. Molecular Ecology, 22, 4606–4618.
Hewitt, G. (2000). The genetic legacy of the quaternary ice ages. Nature, 405, 907–913.
Hewitt, G. M. (1999). Post‐glacial re‐colonization of European biota. Biological Journal of the Linnean Society, 68(1–2), 87–112.
Jakobsson, M., & Rosenberg, N. A. (2007). clumpp: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics, 23(14), 1801–1806.
Jombart, T. (2008). Adegenet: A r package for the multivariate analysis of genetic markers. Bioinformatics, 24(11), 1403–1405.
Kearns, A. M., Restani, M., Szabo, I., Schrøder‐Nielsen, A., Kim, J. A., Richardson, H. M., Marzluff, J. M., Fleischer, R. C., Johnsen, A., & Omland, K. E. (2018). Genomic evidence of speciation reversal in ravens. Nature Communications, 9, 906.
Keightley, P. D., Ness, R. W., Halligan, D. L., & Haddrill, P. R. (2014). Estimation of the spontaneous mutation rate per nucleotide site in a Drosophila melanogaster full‐sib family. Genetics, 196(1), 313–320.
Keller, I., Alexander, J. M., Holderegger, R., & Edwards, P. J. (2013). Widespread phenotypic and genetic divergence along altitudinal gradients in animals. Journal of Evolutionary Biology, 26, 2527–2543.
Kleindorfer, S., O'Connor, J. A., Dudaniec, R. Y., Myers, S. A., Robertson, J., & Sulloway, F. J. (2014). Species collapse via hybridization in Darwin's tree finches. The American Naturalist, 183, 325–341.
Klingenberg, C. P. (2011). MorphoJ: An integrated software package for geometric morphometrics. Molecular Ecology Resources, 11, 353–357.
Körner, C. (2007). The use of ‘altitude’ in ecological research. Trends in Ecology and Evolution, 22, 569–574.
Liu, X. M., & Fu, Y. X. (2020). Stairway Plot 2: Demographic history inference with folded SNP frequency spectra. Genome Biology, 21(1), 280.
Love, S. J., Schweitzer, J. A., Woolbright, S. A., & Bailey, J. K. (2023). Sky islands are a global tool for predicting the ecological and evolutionary consequences of climate change. Annual Review of Ecology, Evolution, and Systematics, 54, 219–236.
Lukicheva, S., & Mardulyn, P. (2021). Whole‐genome sequencing reveals asymmetric introgression between two sister species of cold‐resistant leaf beetles. Molecular Eecology, 30, 4077–4089.
Lutterschmidt, W. I., & Hutchison, V. H. (1997). The critical thermal maximum: History and critique. Canadian Journal of Zoology, 75, 1561–1574.
Maier, P. A., Vandergast, A. G., Ostoja, S. M., Aguilar, A., & Bohonak, A. J. (2019). Pleistocene glacial cycles drove lineage diversification and fusion in the Yosemite toad (Anaxyrus canorus). Evolution, 73, 2476–2496.
Mavárez, J., & Linares, M. (2008). Homoploid hybrid speciation in animals. Molecular Ecology, 17, 4181–4185.
McCulloch, G. A., Foster, B. J., Dutoit, L., Ingram, T., Hay, E., Veale, A. J., Dearden, P. K., & Waters, J. M. (2019). Ecological gradients drive insect wing loss and speciation: The role of the alpine treeline. Molecular Ecology, 28, 3141–3150.
Médail, F., & Quézel, P. (1997). Hot‐spots analysis for conservation of plant biodiversity in the Mediterranean Basin. Annals of the Missouri Botanical Garden, 84, 112–127.
Médail, F., & Quézel, P. (1999). Biodiversity hotspots in the Mediterranean Basin: Setting global conservation priorities. Conservation Biology, 13, 1510–1513.
Millán, A., Picazo, F., Sánchez‐Fernández, D., Abellán, P., & Ribera, I. (2013). Los Coleópteros acuáticos amenazados (Coleoptera). In F. Ruano, M. Tierno de Figueroa, & A. Tinaut (Eds.), Los Insectos de Sierra Nevada. 200 años de historia (pp. 443–456). Asociación Española de Entomología.
Millán, A., Sánchez‐Fernández, D., Abellán, P., Picazo, F., Carbonell, J. A., Lobo, J. M., & Ribera, I. (2014). Atlas de los coleópteros acuáticos de España peninsular. Ministerio de Agricultura, Alimentación y Medio Ambiente.
Miller, K. B., & Bergsten, J. (2016). Diving beetles of the world: Systematics and biology of the Dytiscidae. JHU Press.
Momigliano, P., Florin, A. B., & Merilä, J. (2021). Biases in demographic modeling affect our understanding of recent divergence. Molecular Biology and Evolution, 38(7), 2967–2985.
Muangmai, N., Preuss, M., & Zuccarello, G. C. (2015). Comparative physiological studies on the growth of cryptic species of Bostrychia intricata (Rhodomelaceae, Rhodophyta) in various salinity and temperature conditions. Phycological Research, 63, 300–306.
Múrria, C., Sáinz‐Bariáin, M., Vogler, A. P., Viza, A., González, M., & Zamora‐Muñoz, C. (2020). Vulnerability to climate change for two endemic high‐elevation, low‐dispersive Annitella species (Trichoptera) in Sierra Nevada, the southernmost high mountain in Europe. Insect Conservation and Diversity, 13, 283–295.
Nilsson, A. N., & Hájek, J. (2021). A World Catalogue of the Family Dytiscidae, or the Diving Beetles (Coleoptera, Adephaga). Version 1.I.2021. http://www.waterbeetles.eu.
Nilsson, A. N., & Holmen, M. (1995). The aquatic Adephaga (Coleoptera) of Fennoscandia and Denmark. II. Dytiscidae. Fauna Entomologica Scandinavica, 32, 1–192.
Nilsson, A. N., & Persson, S. (1990). Dimorphism of the metasternal wing in Agabus raffrayi and A. labiatus (Coleoptera: Dytiscidae) questioned. Aquatic Insects, 12, 135–144.
Noguerales, V., Arjona, Y., García‐Olivares, V., Machado, A., López, H., Patiño, J., & Emerson, B. C. (2024). Genetic legacies of mega‐landslides: Cycles of isolation and contact across flank collapses in an oceanic Island. Molecular Ecology, 33(9), e17341.
Noguerales, V., & Ortego, J. (2022). Genomic evidence of speciation by fusion in a recent radiation of grasshoppers. Evolution, 76, 2618–2633.
Ortego, J., Gutiérrez‐Rodríguez, J., & Noguerales, V. (2021). Demographic consequences of dispersal‐related trait shift in two recently diverged taxa of montane grasshoppers. Evolution, 75, 1998–2013.
Ortego, J., & Knowles, L. L. (2022). Geographical isolation versus dispersal: Relictual alpine grasshoppers support a model of interglacial diversification with limited hybridization. Molecular Ecology, 31, 296–312.
Pallarés, S., Carbonell, J. A., Picazo, F., Bilton, D. T., Millán, A., & Abellán, P. (2024). Intraspecific variation of thermal tolerance in freshwater insects along elevational gradients: The case of a widespread diving beetle. bioRxiv. https://doi.org/10.1101/2024.03.04.583263.
Pallarés, S., Millán, A., Mirón, J. M., Velasco, J., Sánchez‐Fernández, D., Botella‐Cruz, M., & Abellán, P. (2020). Assessing the capacity of endemic alpine water beetles to face climate change. Insect Conservation and Diversity, 13, 271–282.
Peterson, B. K., Weber, J. N., Kay, E. H., Fisher, H. S., & Hoekstra, H. E. (2012). Double digest RADseq: An inexpensive method for de novo SNP discovery and genotyping in model and non‐model species. PLoS One, 7(5), e37135.
Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155(2), 945–959.
R Core Team. (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R‐project.org/.
Ribera, I., Castro, A., Díaz, J. A., Garrido, J., Izquierdo, A., Jäch, M. A., & Valladares, L. F. (2011). The geography of speciation in narrow‐range endemics of the ‘Haenydra’ lineage (Coleoptera, Hydraenidae, Hydraena). Journal of Biogeography, 38, 502–516.
Ribera, I., Foster, G. N., & Holt, W. V. (1997). Functional types of diving beetle (Coleoptera: Hygrobiidae and Dytiscidae), as identified by comparative swimming behaviour. Biological Journal of Linnaean Socity, 61, 537–558.
Ribera, I., Hernando, C., & Aguilera, P. (1998). An annotated checklist of the Iberian water beetles (Coleoptera). Zapateri, 8, 43–111.
Ribera, I., & Nilsson, A. (1995). Morphometric patterns among diving beetles (Coleoptera: Noteridae, Hygrobiidae, and Dytiscidae). Canadian Journal of Zoology, 73, 2343–2360.
Ribera, I., & Vogler, A. P. (2004). Speciation of Iberian diving beetles in Pleistocene refugia (Coleoptera, Dytiscidae). Molecular Ecology, 13, 179–193.
Rohlf, F. J. (2015). The tps series of software. Hystrix‐Italian Journal of Mammalogy, 26, 9–12.
Rosenberg, N. A. (2004). Distruct: A program for the graphical display of population structure. Molecular Ecology Notes, 4(1), 137–138.
Ruano, F., Tierno de Figueroa, J., & Tinaut, A. (2013). Los insectos de Sierra Nevada: 2000 años de historia. Asociación Española de Entomología.
Rubalcaba, J. G., Verberk, W. C., Hendriks, A. J., Saris, B., & Woods, H. A. (2020). Oxygen limitation may affect the temperature and size dependence of metabolism in aquatic ectotherms. Proceedings of the National Academy of Sciences, 117(50), 31963–31968.
Schmitt, T. (2007). Molecular biogeography of Europe: Pleistocene cycles and postglacial trends. Frontiers in Zoology, 4, 11.
Schoville, S. D., Roderick, G. K., & Kavanaugh, D. H. (2012). Testing the ‘Pleistocene species pump'in alpine habitats: Lineage diversification of flightless ground beetles (Coleoptera: Carabidae: Nebria) in relation to altitudinal zonation. Biological Journal of the Linnean Society, 107, 95–111.
Seehausen, O. (2006). Conservation: Losing biodiversity by reverse speciation. Current Biology, 16, R334–R337.
Seehausen, O., Takimoto, G., Roy, D., & Jokela, J. (2008). Speciation reversal and biodiversity dynamics with hybridization in changing environments. Molecular Ecology, 17, 30–44.
Shah, A. A., Gill, B. A., Encalada, A. C., Flecker, A. S., Funk, W. C., Guayasamin, J. M., Kondratieff, B. C., Poff, N. L. R., Thomas, S. A., Zamudio, K. R., & Ghalambor, C. K. (2017). Climate variability predicts thermal limits of aquatic insects across elevation and latitude. Functional Ecology, 31(11), 2118–2127.
Sharp, D. (1882). On aquatic carnivorous Coleoptera or Dytiscidae. The Scientific transactions of the Royal Dublin Society, Series 2, 2, 17–1003.
Slatyer, R. A., & Schoville, S. D. (2016). Physiological limits along an elevational gradient in a radiation of montane ground beetles. PLoS One, 11. e0151959.
Sommaruga, R. (2001). The role of solar UV radiation in the ecology of alpine lakes. Journal of Photochemistry and Photobiology B: Biology, 62(1–2), 35–42.
Stanbrook, R., Wheater, C. P., Harris, W. E., & Jones, M. (2021). Habitat type and altitude work in tandem to drive the community structure of dung beetles in Afromontane forest. Journal of Insect Conservation, 25, 159–173.
Stanton, D. W., Frandsen, P., Waples, R. K., Heller, R., Russo, I. R. M., Orozco‐terWengel, P. A., Tingskov Pedersen, C.‐E., Siegismund, H. R., & Bruford, M. W. (2019). More grist for the mill? Species delimitation in the genomic era and its implications for conservation. Conservation Genetics, 20, 101–113.
Steinbauer, M. J., Irl, S. D. H., & Beierkuhnlein, C. (2013). Elevation driven ecological isolation promotes‐diversification on Mediterranean islands. Acta Oecologica, 47, 52–56.
Stevens, G. C. (1989). The latitudinal gradient in geographical range: How so many species coexist in the tropics. The American Naturalist, 133, 240–256.
Stewart, J. R., Lister, A. M., Barnes, I., & Dalen, L. (2010). Refugia revisited: Individualistic responses in space and time. Proceedings of the Royal Society B: Biological Sciences, 277, 661–671.
Swofford, D. L. (2002). PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates.
Taylor, E. B., Boughman, J. W., Groenenboom, M., Sniatynski, M., Schluter, D., & Gow, J. L. (2006). Speciation in reverse: Morphological and genetic evidence of the collapse of a three‐spined stickleback (Gasterosteus aculeatus) species pair. Molecular Ecology, 15, 343–355.
Tonzo, V., & Ortego, J. (2021). Glacial connectivity and current population fragmentation in sky islands explain the contemporary distribution of genomic variation in two narrow‐endemic montane grasshoppers from a biodiversity hotspot. Diversity and Distributions, 27, 1619–1633.
Tonzo, V., Papadopoulou, A., & Ortego, J. (2019). Genomic data reveal deep genetic structure but no support for current taxonomic designation in a grasshopper species complex. Molecular Ecology, 28, 3869–3886.
Tribsch, A. (2004). Areas of endemism of vascular plants in the eastern Alps in relation to Pleistocene glaciation. Journal of Biogeography, 31, 747–760.
Tsuchiya, Y., Takami, Y., Okuzaki, Y., & Sota, T. (2012). Genetic differences and phenotypic plasticity in body size between high‐and low‐altitude populations of the ground beetle Carabus tosanus. Journal of Evolutionary Biology, 25, 1835–1842.
Vonlanthen, P., Bittner, D., Hudson, A. G., Young, K. A., Müller, R., Lundsgaard‐Hansen, B., Roy, D., Di Piazza, S., Largiader, C. R., & Seehausen, O. (2012). Eutrophication causes speciation reversal in whitefish adaptive radiations. Nature, 482, 357–362.
Webb, W. C., Marzluff, J. M., & Omland, K. E. (2011). Random interbreeding between cryptic lineages of the common raven: Evidence for speciation in reverse. Molecular Ecology, 20, 2390–2402.
Weir, B. S., & Cockerham, C. C. (1984). Estimating F‐statistics for the analysis of population structure. Evolution, 38, 1358–1370.
Weir, J. T., & Schluter, D. (2004). Ice sheets promote speciation in boreal birds. Proceedings of the Royal Society B: Biological Sciences, 271, 1881–1887.
Zamora, R., & Oliva, M. (Eds.). (2022). The landscape of the Sierra Nevada: A unique Laboratory of Global Processes in Spain. Springer Nature.
Zelditch, M. L., Swiderski, D. L., Sheets, H. D., & Fink, W. L. (2004). Geometric morphometrics for biologists: A primer. Elsevier Academic Press.
معلومات مُعتمدة: Next Generation EU; PID2019-108895GB-I00 Ministerio de Ciencia e Innovación; 19868 Ministerio de Universidades; SP-DOC_01211 Consejería de Economía, Conocimiento, Empresas y Universidad, Junta de Andalucía
فهرسة مساهمة: Keywords: Coleoptera; Pleistocene speciation; alpine ecosystems; glacial refugia; hybridisation; integrative taxonomy; sky‐islands
تواريخ الأحداث: Date Created: 20240807 Date Completed: 20240827 Latest Revision: 20240827
رمز التحديث: 20240827
DOI: 10.1111/mec.17487
PMID: 39108249
قاعدة البيانات: MEDLINE
الوصف
تدمد:1365-294X
DOI:10.1111/mec.17487