Skip to main content
SpringerLink
Log in

Geographical and Ecological Drivers of Mitonuclear Genetic Divergence in a Mediterranean Grasshopper

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

The study of the neutral and/or selective processes driving genetic variation in natural populations is central to determine the evolutionary history of species and lineages and understand how they interact with different historical and contemporary components of landscape heterogeneity. Here, we combine nuclear and mitochondrial data to study the processes shaping genetic divergence in the Mediterranean esparto grasshopper (Ramburiella hispanica). Our analyses revealed the presence of three main lineages, two in Europe that split in the Early-Middle Pleistocene and one in North Africa that diverged from the two European ones after the Messinian. Lineage-specific potential distribution models and tests of environmental niche differentiation suggest that the phylogeographic structure of the species was driven by allopatric divergence due to the re-opening of the Gibraltar strait at the end of the Messinian (Europe–Africa split) and population fragmentation in geographically isolated Pleistocene climatic refugia (European split). Although we found no evidence for environment as an important driver of genetic divergence at the onset of lineage formation, our analyses considering the spatial distribution of populations and different aspects of landscape composition suggest that genetic differentiation at mitochondrial loci was largely explained by environmental dissimilarity, whereas resistance-based estimates of geographical distance were the only predictors of genetic differentiation at nuclear markers. Overall, our study shows that although historical factors have largely shaped concordant range-wide patterns of mitonuclear genetic structure in the esparto grasshopper, different contemporary processes (neutral gene flow vs. environmental-based selection) seem to be governing the spatial distribution of genetic variation in the two genomes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

(picture by Gilles San Martin). (Color figure online)

Similar content being viewed by others

References

  • Aguirre, M. P., Noguerales, V., Cordero, P. J., & Ortego, J. (2014). Isolation and characterization of polymorphic microsatellites in the specialist grasshopper Ramburiella hispanica (Orthoptera: Acrididae). Conservation Genetics Resources, 6(3), 723–724. doi:10.1007/s12686-014-0198-4.

    Article  Google Scholar 

  • Aljanabi, S. M., & Martinez, I. (1997). Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Research, 25(22), 4692–4693. doi:10.1093/nar/25.22.4692.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Avise, J. (1994). Molecular markers, natural history and evolution. New York: Chapman and Hall.

    Book  Google Scholar 

  • Baele, G., Lemey, P., Bedford, T., Rambaut, A., Suchard, M. A., & Alekseyenko, A. V. (2012). Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Molecular Biology and Evolution, 29(9), 2157–2167. doi:10.1093/molbev/mss084.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ballard, J. W. O., & Kreitman, M. (1994). Unraveling selection in the mitochondrial genome of Drosophila. Genetics, 138(3), 757–772.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ballard, J. W. O., & Whitlock, M. C. (2004). The incomplete natural history of mitochondria. Molecular Ecology, 13(4), 729–744. doi:10.1046/j.1365-294X.2003.02063.x.

    Article  PubMed  Google Scholar 

  • Bar-Yaacov, D., Hadjivasiliou, Z., Levin, L., Barshad, G., Zarivach, R., Bouskila, A., et al. (2015). Mitochondrial involvement in vertebrate speciation? The case of mito-nuclear genetic divergence in chameleons. Genome Biology and Evolution, 7(12), 3322–3336. doi:10.1093/gbe/evv226.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blondel, J., & Aronson, J. (1999). Biology and wildlife of the Mediterranean region. Oxford: Oxford University Press.

    Google Scholar 

  • Bradburd, G. S., Ralph, P. L., & Coop, G. M. (2013). Disentangling the effects of geographic and ecological isolation on genetic differentiation. Evolution, 67(11), 3258–3273. doi:10.1111/evo.12193.

    Article  PubMed  Google Scholar 

  • Brito, P., & Edwards, S. V. (2009). Multilocus phylogeography and phylogenetics using sequence-based markers. Genetica, 135(3), 439–455. doi:10.1007/s10709-008-9293-3.

    Article  PubMed  Google Scholar 

  • Cavalli-Sforza, L. L., & Edwards, A. W. F. (1967). Phylogenetic analysis models and estimation procedures. American Journal of Human Genetics, 19(3P1), 233–257.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chapuis, M. P., & Estoup, A. (2007). Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution, 24(3), 621–631.

    Article  CAS  PubMed  Google Scholar 

  • Chapuis, M. P., Lecoq, M., Michalakis, Y., Loiseau, A., Sword, G. A., Piry, S., et al. (2008). Do outbreaks affect genetic population structure? A worldwide survey in Locusta migratoria, a pest plagued by microsatellite null alleles. Molecular Ecology, 17(16), 3640–3653.

    Article  PubMed  Google Scholar 

  • Cheviron, Z. A., & Brumfield, R. T. (2009). Migration-selection balance and local adaptation of mitochondrial haplotypes in rofous-collared sparrows (Zonotrichia capensis) along an elevational gradient. Evolution, 63(6), 1593–1605. doi:10.1111/j.1558-5646.2009.00644.x.

    Article  PubMed  Google Scholar 

  • Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: More models, new heuristics and parallel computing. Nature Methods, 9(8), 772–772.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29(8), 1969–1973. doi:10.1093/molbev/mss075.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dupanloup, I., Schneider, S., & Excoffier, L. (2002). A simulated annealing approach to define the genetic structure of populations. Molecular Ecology, 11(12), 2571–2581.

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1007/s12686-011-9548-7.

    Article  Google Scholar 

  • Edwards, S., & Bensch, S. (2009). Looking forwards or looking backwards in avian phylogeography? A comment on Zink and Barrowclough 2008. Molecular Ecology, 18(14), 2930–2933. doi:10.1111/j.1365-294X.2009.04270.x.

    Article  CAS  PubMed  Google Scholar 

  • Elith, J., Phillips, S. J., Hastie, T., Dudik, M., Chee, Y. E., & Yates, C. J. (2011). A statistical explanation of MaxEnt for ecologists. Diversity and Distributions, 17(1), 43–57. doi:10.1111/j.1472-4642.2010.00725.x.

    Article  Google Scholar 

  • Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Molecular Ecology, 14(8), 2611–2620. doi:10.1111/j.1365-294X.2005.02553.x.

    Article  CAS  PubMed  Google Scholar 

  • Excoffier, L., Laval, G., & Schneider, S. (2005). Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47–50.

    CAS  Google Scholar 

  • Faille, A., Andujar, C., Fadrique, F., & Ribera, I. (2014). Late Miocene origin of an Ibero-Maghrebian clade of ground beetles with multiple colonizations of the subterranean environment. Journal of Biogeography, 41(10), 1979–1990. doi:10.1111/jbi.12349.

    Article  Google Scholar 

  • Ferrer, E. S., Garcia-Navas, V., Bueno-Enciso, J., Barrientos, R., Serrano-Davies, E., Caliz-Campal, C., et al. (2016). The influence of landscape configuration and environment on population genetic structure in a sedentary passerine: Insights from loci located in different genomic regions. Journal of Evolutionary Biology, 29(1), 205–219. doi:10.1111/jeb.12776.

    Article  CAS  PubMed  Google Scholar 

  • Folmer, O., Black, M., Hoeh, W., Lutz, R., & Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–299.

    CAS  PubMed  Google Scholar 

  • Fontanillas, P., Depraz, A., Giorgi, M. S., & Perrin, N. (2005). Nonshivering thermogenesis capacity associated to mitochondrial DNA haplotypes and gender in the greater white-toothed shrew, Crocidura russula. Molecular Ecology, 14(2), 661–670. doi:10.1111/j.1365-294X.2004.02414.x.

    Article  CAS  PubMed  Google Scholar 

  • Fu, Y. X. (1997). Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147(2), 915–925.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Galtier, N., Nabholz, B., Glemin, S., & Hurst, G. D. D. (2009). Mitochondrial DNA as a marker of molecular diversity: A reappraisal. Molecular Ecology, 18(22), 4541–4550. doi:10.1111/j.1365-294X.2009.04380.x.

    Article  CAS  PubMed  Google Scholar 

  • Gaspari, S., Scheinin, A., Holcer, D., Fortuna, C., Natali, C., Genov, T., et al. (2015). Drivers of population structure of the bottlenose dolphin (Tursiops truncatus) in the Eastern Mediterranean sea. Evolutionary Biology, 42(2), 177–190. doi:10.1007/s11692-015-9309-8.

    Article  Google Scholar 

  • Gotelli, N. J., & Stanton-Geddes, J. (2015). Climate change, genetic markers and species distribution modelling. Journal of Biogeography, 42(9), 1577–1585. doi:10.1111/jbi.12562.

    Article  Google Scholar 

  • Graham, C. H., Ron, S. R., Santos, J. C., Schneider, C. J., & Moritz, C. (2004). Integrating phylogenetics and environmental niche models to explore speciation mechanisms in dendrobatid frogs. Evolution, 58(8), 1781–1793. doi:10.1554/03-274.

    Article  PubMed  Google Scholar 

  • Guo, S. W., & Thompson, E. A. (1992). A monte-carlo method for combined segregation and linkage analysis. American Journal of Human Genetics, 51(5), 1111–1126.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hasumi, H., & Emori, S. (2004). K-1 coupled GCM (MIROC) description. Center for Climate System Research, University of Tokyo, National Institute for Environmental Studies, Frontier Research Center for Global Change, Tokyo.

  • Hewitt, G. (2000). The genetic legacy of the Quaternary ice ages. Nature, 405(6789), 907–913.

    Article  CAS  PubMed  Google Scholar 

  • 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(1442), 183–195.

    Article  CAS  Google Scholar 

  • Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G., & Jarvis, A. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25(15), 1965–1978. doi:10.1002/joc.1276.

    Article  Google Scholar 

  • Hubisz, M. J., Falush, D., Stephens, M., & Pritchard, J. K. (2009). Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources, 9(5), 1322–1332. doi:10.1111/j.1755-0998.2009.02591.x.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hutchison, D. W., & Templeton, A. R. (1999). Correlation of pairwise genetic and geographic distance measures: Inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution, 53(6), 1898–1914.

    Article  PubMed  Google Scholar 

  • 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. doi:10.1093/bioinformatics/btm233.

    Article  CAS  PubMed  Google Scholar 

  • Kiehl, J. T., & Gent, P. R. (2004). The community climate system model, version 2. Journal of Climate, 17(19), 3666–3682.

    Article  Google Scholar 

  • Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide-sequences. Journal of Molecular Evolution, 16(2), 111–120. doi:10.1007/bf01731581.

    Article  CAS  PubMed  Google Scholar 

  • Krijgsman, W., Hilgen, F. J., Raffi, I., Sierro, F. J., & Wilson, D. S. (1999). Chronology, causes and progression of the Messinian salinity crisis. Nature, 400(6745), 652–655.

    Article  CAS  Google Scholar 

  • Kumar, A., Ghazi, M. G. U., Hussain, S. A., Bhatt, D., & Gupta, S. K. (2017). Mitochondrial and nuclear DNA based genetic assessment indicated distinct variation and low genetic exchange among the three subspecies of swamp deer (Rucervus duvaucelii). Evolutionary Biology, 44(1), 31–42. doi:10.1007/s11692-016-9387-2.

    Article  Google Scholar 

  • Langella, O. (1999). Populations 1.2.31 software. http://bioinformatics.org/populations/. Accessed 2 Oct 2016.

  • Latorre-Pellicer, A., Moreno-Loshuertos, R., Lechuga-Vieco, A. V., Sanchez-Cabo, F., Torroja, C., Acin-Perez, R., et al. (2016). Mitochondrial and nuclear DNA matching shapes metabolism and healthy ageing. Nature, 535(7613), 561–565. doi:10.1038/nature18618.

    Article  CAS  PubMed  Google Scholar 

  • Lee, C. R., & Mitchell-Olds, T. (2011). Quantifying effects of environmental and geographical factors on patterns of genetic differentiation. Molecular Ecology, 20(22), 4631–4642. doi:10.1111/j.1365-294X.2011.05310.x.

    Article  PubMed  PubMed Central  Google Scholar 

  • Librado, P., & Rozas, J. (2009). DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25(11), 1451–1452. doi:10.1093/bioinformatics/btp187.

    Article  CAS  PubMed  Google Scholar 

  • Llucià-Pomares, D. (2002). Revision of the Orthoptera (Insecta) of Catalonia (Spain). Monografias SEA, 7, 1–226.

    Google Scholar 

  • Magalhaes, I. L. F., Oliveira, U., Santos, F. R., Vidigal, T., Brescovit, A. D., & Santos, A. J. (2014). Strong spatial structure, Pliocene diversification and cryptic diversity in the Neotropical dry forest spider Sicarius cariri. Molecular Ecology, 23(21), 5323–5336. doi:10.1111/mec.12937.

    Article  PubMed  Google Scholar 

  • Martin, M. D., & Mendelson, T. C. (2012). Signal divergence is correlated with genetic distance and not environmental differences in darters (Percidae: Etheostoma). Evolutionary Biology, 39(2), 231–241. doi:10.1007/s11692-012-9179-2.

    Article  Google Scholar 

  • Massatti, R., & Knowles, L. L. (2014). Microhabitat differences impact phylogeographic concordance of codistributed species: Genomic evidence in montane sedges (Carex L.) from the Rocky Mountains. Evolution, 68(10), 2833–2846. doi:10.1111/evo.12491.

    Article  PubMed  Google Scholar 

  • McCormack, J. E., Zellmer, A. J., & Knowles, L. L. (2010). Does niche divergence accompany allopatric divergence in Aphelocoma jays as predicted under ecological speciation?: Insights from tests with niche models. Evolution, 64(5), 1231–1244. doi:10.1111/j.1558-5646.2009.00900.x.

    PubMed  Google Scholar 

  • McDonald, J. H., & Kreitman, M. (1991). Adaptive protein evolution at the ADH locus in Drosophila. Nature, 351(6328), 652–654. doi:10.1038/351652a0.

    Article  CAS  PubMed  Google Scholar 

  • McRae, B. H. (2006). Isolation by resistance. Evolution, 60(8), 1551–1561. doi:10.1111/j.0014-3820.2006.tb00500.x.

    Article  PubMed  Google Scholar 

  • McRae, B. H., & Beier, P. (2007). Circuit theory predicts gene flow in plant and animal populations. Proceedings of the National Academy of Sciences of the United States of America, 104(50), 19885–19890. doi:10.1073/pnas.0706568104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McRae, B. H., Dickson, B. G., Keitt, T. H., & Shah, V. B. (2008). Using circuit theory to model connectivity in ecology, evolution, and conservation. Ecology, 89(10), 2712–2724. doi:10.1890/07-1861.1.

    Article  PubMed  Google Scholar 

  • Meiklejohn, C. D., Montooth, K. L., & Rand, D. M. (2007). Positive and negative selection on the mitochondrial genome. Trends in Genetics, 23(6), 259–263. doi:10.1016/j.tig.2007.03.008.

    Article  CAS  PubMed  Google Scholar 

  • Morales, H. E., Pavlova, A., Joseph, L., & Sunnucks, P. (2015). Positive and purifying selection in mitochondrial genomes of a bird with mitonuclear discordance. Molecular Ecology, 24(11), 2820–2837. doi:10.1111/mec.13203.

    Article  CAS  PubMed  Google Scholar 

  • Moritz, C. C., & Potter, S. (2013). The importance of an evolutionary perspective in conservation policy planning. Molecular Ecology, 22(24), 5969–5971. doi:10.1111/mec.12565.

    Article  PubMed  Google Scholar 

  • Nakazato, T., Warren, D. L., & Moyle, L. C. (2010). Ecological and geographic models of species divergence in wild tomatoes. American Journal of Botany, 97(4), 680–693. doi:10.3732/ajb.0900216.

    Article  PubMed  Google Scholar 

  • Noguerales, V., Cordero, P. J., & Ortego, J. (2016). Hierarchical genetic structure shaped by topography in a narrow-endemic montane grasshopper. BMC Evolutionary Biology, 16, 96. doi:10.1186/s12862-016-0663-7.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nosil, P. (2012). Ecological speciation. New York: Oxford University Press.

    Book  Google Scholar 

  • Novicic, Z. K., Immonen, E., Jelic, M., Andelkovic, M., Stamenkovic-Radak, M., & Arnqvist, G. (2015). Within-population genetic effects of mtDNA on metabolic rate in Drosophila subobscura. Journal of Evolutionary Biology, 28(2), 338–346. doi:10.1111/jeb.12565.

    Article  Google Scholar 

  • Ortego, J., Aguirre, M. P., Noguerales, V., & Cordero, P. J. (2015a). Consequences of extensive habitat fragmentation in landscape-level patterns of genetic diversity and structure in the Mediterranean esparto grasshopper. Evolutionary Applications, 8(6), 621–632. doi:10.1111/eva.12273.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ortego, J., Garcia-Navas, V., Noguerales, V., & Cordero, P. J. (2015b). Discordant patterns of genetic and phenotypic differentiation in five grasshopper species codistributed across a microreserve network. Molecular Ecology, 24(23), 5796–5812. doi:10.1111/mec.13426.

    Article  PubMed  Google Scholar 

  • Palumbi, S. R., Martin, A., Romano, S. L., McMillian, W. O., Stice, L., & Grabowski, G. (1991). The simple Fool’s guide to PCR, version 2.0. Honolulu: University of Hawaii

    Google Scholar 

  • Papadopoulou, A., Anastasiou, I., & Vogler, A. P. (2010). Revisiting the insect mitochondrial molecular clock: The Mid-Aegean trench calibration. Molecular Biology and Evolution, 27(7), 1659–1672. doi:10.1093/molbev/msq051.

    Article  CAS  PubMed  Google Scholar 

  • Pavlova, A., Amos, J. N., Joseph, L., Loynes, K., Austin, J. J., Keogh, J. S., et al. (2013). Perched at the mito-nuclear crossroads: Divergent mitochondrial lineages correlate with environment in the face of ongoing nuclear gene flow in an Australian bird. Evolution, 67(12), 3412–3428. doi:10.1111/evo.12107.

    Article  CAS  PubMed  Google Scholar 

  • Phillips, S. J., Anderson, R. P., & Schapire, R. E. (2006). Maximum entropy modeling of species geographic distributions. Ecological Modelling, 190(3–4), 231–259. doi:10.1016/j.ecolmodel.2005.03.026.

    Article  Google Scholar 

  • Phillips, S. J., & Dudik, M. (2008). Modeling of species distributions with Maxent: New extensions and a comprehensive evaluation. Ecography, 31(2), 161–175. doi:10.1111/j.0906-7590.2008.5203.x.

    Article  Google Scholar 

  • Pichaud, N., Ballard, J. W. O., Tanguay, R. M., & Blier, P. U. (2012). Naturally occurring mitochondrial DNA haplotypes exhibit metabolic differences: Insight into functional properties of mitochondria. Evolution, 66(10), 3189–3197. doi:10.1111/j.1558-5646.2012.01683.x.

    Article  CAS  PubMed  Google Scholar 

  • Pinho, C., Ferrand, N., & Harris, D. J. (2006). Reexamination of the Iberian and North African Podarcis (Squamata: Lacertidae) phylogeny based on increased mitochondrial DNA sequencing. Molecular Phylogenetics and Evolution, 38(1), 266–273. doi:10.1016/j.ympev.2005.06.012.

    Article  CAS  PubMed  Google Scholar 

  • Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155(2), 945–959.

    CAS  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2016). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

    Google Scholar 

  • Ribeiro, A. M., Lloyd, P., & Bowie, R. C. K. (2011). A tight balance between natural selection and gene flow in a souhern African arid-zone endemic bird. Evolution, 65(12), 3499–3514. doi:10.1111/j.1558-5646.2011.01397.x.

    Article  PubMed  Google Scholar 

  • Rosenberg, N. A. (2004). DISTRUCT: A program for the graphical display of population structure. Molecular Ecology Notes, 4(1), 137–138. doi:10.1046/j.1471-8286.2003.00566.x.

    Article  Google Scholar 

  • Rosetti, N., & Remis, M. I. (2017). Variability of minisatellite loci and mtDNA in individuals with and without B chromosomes from populations of the grasshopper Dichroplus elongatus. Evolutionary Biology, 44(2), 273–283. doi:10.1007/s11692-016-9406-3.

    Article  Google Scholar 

  • Sanmartín, I. (2003). Dispersal vs. vicariance in the Mediterranean: Historical biogeography of the Palearctic Pachydeminae (Coleoptera, Scarabaeoidea). Journal of Biogeography, 30(12), 1883–1897.

    Article  Google Scholar 

  • Schoener, T. W. (1968). Anolis lizards of Bimini—Resource partitioning in a complex fauna. Ecology, 49(4), 704–726. doi:10.2307/1935534.

    Article  Google Scholar 

  • Sexton, J. P., Hangartner, S. B., & Hoffmann, A. A. (2014). Genetic isolation by environment or distance: Which patterns of gene flow is most common? Evolution, 68(1), 1–15. doi:10.1111/evo.12258.

    Article  CAS  PubMed  Google Scholar 

  • Shafer, A. B. A., & Wolf, J. B. W. (2013). Widespread evidence for incipient ecological speciation: A meta-analysis of isolation-by-ecology. Ecology Letters, 16(7), 940–950. doi:10.1111/ele.12120.

    Article  PubMed  Google Scholar 

  • Singhal, S., & Moritz, C. (2012). Strong selection against hybrids maintains a narrow contact zone between morphologically cryptic lineages in a rainforest lizard. Evolution, 66(5), 1474–1489, doi:10.1111/j.1558-5646.2011.01539.x.

    Article  PubMed  Google Scholar 

  • Slatkin, M. (1993). Isolation by distance in equilibrium and nonequilibrium populations. Evolution, 47(1), 264–279.

    Article  PubMed  Google Scholar 

  • Soria-Carrasco, V., Gompert, Z., Comeault, A. A., Farkas, T. E., Parchman, T. L., Johnston, J. S., et al. (2014). Stick insect genomes reveal natural selection’s role in parallel speciation. Science, 344(6185), 738–742. doi:10.1126/science.1252136.

    Article  CAS  PubMed  Google Scholar 

  • Sun, J. T., Wang, M. M., Zhang, Y. K., Chapuis, M. P., Jiang, X. Y., Hu, G., et al. (2015). Evidence for high dispersal ability and mito-nuclear discordance in the small brown planthopper, Laodelphax striatellus. Scientific Reports. doi:10.1038/srep08045.

    Google Scholar 

  • Tajima, F. (1989). Statistical-method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123(3), 585–595.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Takezaki, N., & Nei, M. (1996). Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA. Genetics, 144(1), 389–399.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thorpe, R. S., Surget-Groba, Y., & Johansson, H. (2008). The relative importance of ecology and geographic isolation for speciation in anoles. Philosophical Transactions of the Royal Society B-Biological Sciences, 363(1506), 3071–3081. doi:10.1098/rstb.2008.0077.

    Article  PubMed Central  Google Scholar 

  • Toews, D. P. L., & Brelsford, A. (2012). The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology, 21(16), 3907–3930. doi:10.1111/j.1365-294X.2012.05664.x.

    Article  CAS  PubMed  Google Scholar 

  • Wang, I. J. (2013). Examining the full effects of landscape heterogeneity on spatial genetic variation: A multiple matrix regression approach for quantifying geographic and ecological isolation. Evolution, 67(12), 3403–3411. doi:10.1111/evo.12134.

    Article  PubMed  Google Scholar 

  • Wang, I. J., & Bradburd, G. S. (2014). Isolation by environment. Molecular Ecology, 23(23), 5649–5662. doi:10.1111/mec.12938.

    Article  PubMed  Google Scholar 

  • Wang, I. J., Glor, R. E., & Losos, J. B. (2013). Quantifying the roles of ecology and geography in spatial genetic divergence. Ecology Letters, 16(2), 175–182. doi:10.1111/ele.12025.

    Article  PubMed  Google Scholar 

  • Warren, D. L., Glor, R. E., & Turelli, M. (2008). Environmental niche equivalency versus conservatism: Quantitative approaches to niche evolution. Evolution, 62(11), 2868–2883. doi:10.1111/j.1558-5646.2008.00482.x.

    Article  PubMed  Google Scholar 

  • Wright, S. (1943). Isolation by distance. Genetics, 28(2), 114–138.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zink, R. M., & Barrowclough, G. F. (2008). Mitochondrial DNA under siege in avian phylogeography. Molecular Ecology, 17(9), 2107–2121. doi:10.1111/j.1365-294X.2008.03737.x.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We wish to thank to Conchi Cáliz for her valuable help in sample collection and genotyping. Two anonymous referees provided valuable comments on an earlier draft of this manuscript. JO was supported by “Ramón y Cajal” (RYC-2013-12501) and “Severo Ochoa” (SEV-2012-0262) research fellowships. VN was supported by a FPI pre-doctoral fellowship (BES-2012-053741). This work received financial support from Ministerio de Economía y Competitividad (Grants CGL2011-25053 and CGL2014-54671-P), Junta de Comunidades de Castilla-La Mancha and European Social Fund (Grants PCI08-0130-3954, POII10-0197-0167 and PEII-2014-023-P), and European Regional Development Fund (Grant UNCM08-1E-018).

Author information

Authors and Affiliations

  1. Department of Integrative Ecology, Estación Biológica de Doñana, EBD-CSIC, Avda. Américo Vespucio 26, 41092, Seville, Spain

    J. Ortego

  2. Grupo de Investigación de la Biodiversidad Genética y Cultural, Instituto de Investigación en Recursos Cinegéticos - IREC (CSIC, UCLM, JCCM), Ronda de Toledo 12, 13071, Ciudad Real, Spain

    V. Noguerales & P. J. Cordero

Authors
  1. J. Ortego
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. Noguerales
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. J. Cordero
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. Ortego.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 1073 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ortego, J., Noguerales, V. & Cordero, P.J. Geographical and Ecological Drivers of Mitonuclear Genetic Divergence in a Mediterranean Grasshopper. Evol Biol 44, 505–521 (2017). https://doi.org/10.1007/s11692-017-9423-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-017-9423-x

Keywords

Search

Navigation