Hierarchical genetic structure shaped by topography in a narrow-endemic montane grasshopper

BMC Evolutionary Biology

Volumn 16, Issue 1, 2016, Pages

  Noguerales, Víctor ^a   Cordero, Pedro J ^a   Ortego, Joaquín ^b  

^a INSTITUTO DE INVESTIGACIÓN EN RECURSOS CINEGÉTICOS IREC CSIC UCLM JCCM   (Spain)

^b DEPARTMENT OF CONSERVATION BIOLOGY   (Spain)

Author keywords

Chorthippus saulcyi moralesi; Ecological niche modelling; Hierarchical genetic structure; Isolation by environment; Isolation by resistance; Landscape genetics; Pyrenees; Topographic complexity

Indexed keywords

CLIMATE CHANGE; DISPERSAL; DIVERGENCE; ECOLOGICAL MODELING; ENVIRONMENTAL CHANGE; EVOLUTIONARY BIOLOGY; GENETIC ANALYSIS; GENETIC DIFFERENTIATION; GENETIC STRUCTURE; GENETIC VARIATION; GRASSHOPPER; HABITAT CORRIDOR; HETEROGENEITY; LANDSCAPE ECOLOGY; MICROHABITAT; TOPOGRAPHY;

PYRENEES;

CHORTHIPPUS;

MICROSATELLITE DNA;

ANIMAL; BIOLOGICAL MODEL; CAELIFERA; CLIMATE; CLUSTER ANALYSIS; ECOSYSTEM; FRANCE; GENE; GENE FLOW; GENETIC DRIFT; GENETIC VARIATION; GENETICS; MOLECULAR EVOLUTION; PHYLOGEOGRAPHY;

ANIMALS; CLIMATE; CLUSTER ANALYSIS; ECOSYSTEM; EVOLUTION, MOLECULAR; FRANCE; GENE FLOW; GENES, INSECT; GENETIC DRIFT; GENETIC VARIATION; GRASSHOPPERS; MICROSATELLITE REPEATS; MODELS, GENETIC; PHYLOGEOGRAPHY;

EID: 84969622687     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/s12862-016-0663-7     Document Type: Article

References (103)

1. Carnaval AC, Hickerson MJ, Haddad CFB, Rodrigues MT, Moritz C. Stability predicts genetic diversity in the Brazilian Atlantic forest hotspot. Science. 2009;323:785-9.
2. Yannic G, Pellissier L, Ortego J, Lecomte N, Couturier S, Cuyler C, et al. Genetic diversity in caribou linked to past and future climate change. Nat Clim Change. 2014;4:132-7.
3. Lee CR, Mitchell-Olds T. Quantifying effects of environmental and geographical factors on patterns of genetic differentiation. Mol Ecol. 2011;20:4631-42.
4. Shafer ABA, Wolf JBW. Widespread evidence for incipient ecological speciation: a meta-analysis of isolation-by-ecology. Ecol Lett. 2013;16:940-50.
5. Wang IJ, Glor RE, Losos JB. Quantifying the roles of ecology and geography in spatial genetic divergence. Ecol Lett. 2013;16:175-82.
6. Wright S. Isolation by distance. Genetics. 1943;28:114-38.
7. Slatkin M. Isolation by distance in equilibrium and nonequilibrium populations. Evolution. 1993;47:264-79.
8. Jenkins DG, Carey M, Czerniewska J, Fletcher J, Hether T, Jones A, et al. A meta-analysis of isolation by distance: relic or reference standard for landscape genetics? Ecography. 2010;33:315-20.
9. Manel S, Holderegger R. Ten years of landscape genetics. Trends Ecol Evol. 2013;28:614-21.
10. Manel S, Schwartz MK, Luikart G, Taberlet P. Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol. 2003;18:189-97.
11. McRae BH. Isolation by resistance. Evolution. 2006;60:1551-61.
12. McRae BH, Beier P. Circuit theory predicts gene flow in plant and animal populations. Proc Natl Acad Sci U S A. 2007;104:19885-90.
13. Ruiz-Gonzalez A, Cushman SA, Madeira MJ, Randi E, Gómez-Moliner BJ. Isolation by distance, resistance and/or clusters? Lessons learned from a forest-dwelling carnivore inhabiting a heterogeneous landscape. Mol Ecol. 2015;24:5110-29.
14. Ortego J, Aguirre MP, Noguerales V, Cordero PJ. Consequences of extensive habitat fragmentation in landscape-level patterns of genetic diversity and structure in the Mediterranean esparto grasshopper. Evol Appl. 2015;8:621-32.
15. Wang IJ, Bradburd GS. Isolation by environment. Mol Ecol. 2014;23:5649-62.
16. Nosil P, Vines TH, Funk DJ. Reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution. 2005;59:705-19.
17. Nosil P. Ecological speciation. New York: Oxford University Press; 2012.
18. Sexton JP, Hangartner SB, Hoffmann AA. Genetic isolation by environment or distance: which pattern of gene flow is most common? Evolution. 2014;68:1-15.
19. Funk DJ, Nosil P, Etges WJ. Ecological divergence exhibits consistently positive associations with reproductive isolation across disparate taxa. Proc Natl Acad Sci U S A. 2006;103:3209-13.
20. Crispo E, Bentzen P, Reznick DN, Kinnison MT, Hendry AP. The relative influence of natural selection and geography on gene flow in guppies. Mol Ecol. 2006;15:49-62.
21. Edwards DL, Keogh JS, Knowles LL. Effects of vicariant barriers, habitat stability, population isolation and environmental features on species divergence in the south-western Australian coastal reptile community. Mol Ecol. 2012;21:3809-22.
22. Meirmans PG. The trouble with isolation by distance. Mol Ecol. 2012;21:2839-46.
23. Balkenhol N, Waits LP, Dezzani RJ. Statistical approaches in landscape genetics: an evaluation of methods for linking landscape and genetic data. Ecography. 2009;32:818-30.
24. Wang IJ. Examining the full effects of landscape heterogeneity on spatial genetic variation: a multiple matrix regression approach for quantifying geographic and ecological isolation. Evolution. 2013;67:3403-11.
25. Botta F, Eriksen C, Fontaine MC, Guillot G. Enhanced computational methods for quantifying the effect of geographic and environmental isolation on genetic differentiation. Methods Ecol Evol. 2015;6:1270-7.
26. Kierepka EM, Latch EK. Performance of partial statistics in individual-based landscape genetics. Mol Ecol Resour. 2015;15:512-25.
27. Forester BR, Jones MR, Joost S, Landguth EL, Lasky JR. Detecting spatial genetic signatures of local adaptation in heterogeneous landscapes. Mol Ecol. 2016;25:104-20.
28. Ferrer ES, García-Navas V, Bueno-Enciso J, Barrientos R, Serrano-Davies E, Cáliz-Campal C, et al. The influence of landscape configuration and environment on population genetic structure in a sedentary passerine: insights from loci located in different genomic regions. J Evol Biol. 2016;29:205-19.
29. Munshi-South J, Zolnik CP, Harris S. Population genomics of the Anthropocene: urbanization is negatively associated with genome-wide variation in white-footed mouse populations. Evol Appl. 2016;9:546-64.
30. Defaut B. Preliminary revision of Chorthippus of the binotatus group (Charpentier, 1825) (Caelifera, Acrididae, Gomphocerinae). Materiaux Orthopteriques et Entomocenotiques. 2011;16:17-54.
31. Llucia-Pomares D. Revision of the Orthoptera (Insecta) of Catalonia (Spain). Monografias SEA, vol. 7. Zaragoza: Sociedad Entomológica Aragonesa; 2002.
32. García-Barros E, Gurrea P, Luciañez MJ, Cano JM, Munguira ML, Moreno JC, et al. Parsimony analysis of endemicity and its application to animal and plant geographical distributions in the Ibero-Balearic region (western Mediterranean). J Biogeogr. 2002;29:109-24.
33. Jiménez-Sánchez M, Rodríguez-Rodríguez L, García-Ruiz JM, Domínguez-Cuesta MJ, Farias P, Valero-Garcés B, et al. A review of glacial geomorphology and chronology in northern Spain: timing and regional variability during the last glacial cycle. Geomorphology. 2013;196:50-64.
34. Hewitt G. The genetic legacy of the Quaternary ice ages. Nature. 2000;405:907-13.
35. Wang IJ. Environmental and topographic variables shape genetic structure and effective population sizes in the endangered Yosemite toad. Divers Distrib. 2012;18:1033-41.
36. Castillo JA, Epps CW, Davis AR, Cushman SA. Landscape effects on gene flow for a climate-sensitive montane species, the American pika. Mol Ecol. 2014;23:843-56.
37. Sobel JM, Chen GF, Watt LR, Schemske DW. The biology of speciation. Evolution. 2010;64:295-315.
38. Legendre P, Anderson MJ. Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr. 1999;69:1-24.
39. Pflüeger FJ, Balkenhol N. A plea for simultaneously considering matrix quality and local environmental conditions when analysing landscape impacts on effective dispersal. Mol Ecol. 2014;23:2146-56.
40. Aljanabi SM, Martínez I. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res. 1997;25:4692-3.
41. Basiita RK, Bruggemann JH, Cai N, Cáliz-Campal C, Chen C, Chen J, et al. Microsatellite records for volume 7, issue 4. Conserv Genet Resour. 2015;7:917-44.
42. Guo SW, Thompson EA. A Monte-Carlo method for combined segregation and linkage analysis. Am J Hum Genet. 1992;51:1111-26.
43. Excoffier L, Lischer HEL. ARLEQUIN suite version 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 2010;10:564-7.
44. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes. 2004;4:535-8.
45. Rice WR. Analyzing tables of statistical tests. Evolution. 1989;43:223-5.
46. Chapuis MP, Lecoq M, Michalakis Y, Loiseau A, Sword GA, Piry S, et al. Do outbreaks affect genetic population structure? A worldwide survey in Locusta migratoria, a pest plagued by microsatellite null alleles. Mol Ecol. 2008;17:3640-53.
47. Chapuis MP, Estoup A. Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol. 2007;24:621-31.
48. Falush D, Stephens M, Pritchard JK. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics. 2003;164:1567-87.
49. Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155:945-59.
50. Papadopoulou A, Knowles LL. Genomic tests of the species-pump hypothesis: recent island connectivity cycles drive population divergence but not speciation in Caribbean crickets across the Virgin Islands. Evolution. 2015;69:1501-17.
51. Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005;14:2611-20.
52. Jakobsson M, Rosenberg NA. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics. 2007;23:1801-6.
53. Rosenberg NA. DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes. 2004;4:137-8.
54. Jombart T, Devillard S, Balloux F. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet. 2010;11:94.
55. R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2014. http://www.R-project.org/. Accessed 29 Dec 2014.
56. Langella O. POPULATIONS 1.2.31 software. 1999. http://bioinformatics.org/populations/. Accessed 25 Feb 2015.
57. Cavalli-Sforza L, Edwards AWF. Phylogenetic analyses: models and estimation procedures. Evolution. 1967;21:550-70.
58. Takezaki N, Nei M. Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA. Genetics. 1996;144:389-99.
59. Phillips SJ, Anderson RP, Schapire RE. Maximum entropy modeling of species geographic distributions. Ecol Model. 2006;190:231-59.
60. Phillips SJ, Dudik M. Modeling of species distributions with MAXENT: new extensions and a comprehensive evaluation. Ecography. 2008;31:161-75.
61. WorldClim: Global Climate Data. http://www.worldclim.org/. Accessed 17 Oct 2015.
62. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. Very high resolution interpolated climate surfaces for global land areas. Int J Climatol. 2005;25:1965-78.
63. Collins WD, Bitz CM, Blackmon ML, Bonan GB, Bretherton CS, Carton JA, et al. The Community Climate System Model version 3 (CCSM3). J Clim. 2006;19:2122-43.
64. Braconnot P, Otto-Bliesner B, Harrison S, Joussaume S, Peterchmitt JY, Abe-Ouchi A, et al. Results of PMIP2 coupled simulations of the Mid-Holocene and Last Glacial Maximum - part 1: experiments and large-scale features. Clim Past. 2007;3:261-77.
65. Otto-Bliesner BL, Marsha SJ, Overpeck JT, Miller GH, Hu AX. CAPE Last Interglacial Project Members. Simulating arctic climate warmth and icefield retreat in the last interglaciation. Science. 2006;311:1751-3.
66. Anderson RP, Raza A. The effect of the extent of the study region on GIS models of species geographic distributions and estimates of niche evolution: preliminary tests with montane rodents (genus Nephelomys) in Venezuela. J Biogeogr. 2010;37:1378-93.
67. Alvarado-Serrano DF, Knowles LL. Ecological niche models in phylogeographic studies: applications, advances and precautions. Mol Ecol Resour. 2014;14:233-48.
68. Elith J, Kearney M, Phillips S. The art of modelling range-shifting species. Methods Ecol Evol. 2010;1:330-42.
69. Lanier HC, Massatti R, He Q, Olson LE, Knowles LL. Colonization from divergent ancestors: glaciation signatures on contemporary patterns of genomic variation in Collared Pikas (Ochotona collaris). Mol Ecol. 2015;24:3688-705.
70. Massatti R, Knowles LL. Microhabitat differences impact phylogeographic concordance of codistributed species: genomic evidence in montane sedges (Carex L.) from the rocky mountains. Evolution. 2014;68:2833-46.
71. Jenness JS. DEM SURFACE TOOLS. Jenness Enterprises. 2013. http://www.jennessent.com/arcgis/surface-area.htm. Accessed 15 Jun 2015
72. Jenness JS. Calculating landscape surface area from digital elevation models. Wildlife Soc B. 2004;32:829-39.
73. NASA Shuttle Radar Topographic Mission: SRTM Digital Elevation Data. 2015. http://srtm.csi.cgiar.org/. Accessed 15 Jun 2015
74. McRae BH, Dickson BG, Keitt TH, Shah VB. Using circuit theory to model connectivity in ecology, evolution, and conservation. Ecology. 2008;89:2712-24.
75. Jha S, Kremen C. Urban land use limits regional bumble bee gene flow. Mol Ecol. 2013;22:2483-95.
76. Velo-Antón G, Parra JL, Parra-Olea G, Zamudio KR. Tracking climate change in a dispersal-limited species: reduced spatial and genetic connectivity in a montane salamander. Mol Ecol. 2013;22:3261-78.
77. Ortego J, Gugger PF, Sork VL. Climatically stable landscapes predict patterns of genetic structure and admixture in the Californian canyon live oak. J Biogeogr. 2015;42:328-38.
78. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB et al. VEGAN: community ecology package. R Package Version 2.3-1. 2015. http://r-forge.r-project.org/projects/vegan. Accessed 22 Nov 2015.
79. Erst PJ. GEOGRAPHIC DISTANCE MATRIX GENERATOR, version 1.2.3. American Museum of Natural History, Center for Biodiversity and Conservation. http://biodiversityinformatics.amnh.org/open-source/gdmg. Accessed 15 Nov 2015.
80. Bradburd GS, Ralph PL, Coop GM. Disentangling the effects of geographic and ecological isolation on genetic differentiation. Evolution. 2013;67:3258-73.
81. Ortego J, Aguirre MP, Cordero PJ. Genetic and morphological divergence at different spatiotemporal scales in the grasshopper Mioscirtus wagneri (Orthoptera: Acrididae). J Insect Conserv. 2012;16:103-10.
82. Ortego J, Aguirre MP, Cordero PJ. Population genetics of Mioscirtus wagneri, a grasshopper showing a highly fragmented distribution. Mol Ecol. 2010;19:472-83.
83. Rizzo V, Comas J, Fadrique F, Fresneda J, Ribera I. Early Pliocene range expansion of a clade of subterranean Pyrenean beetles. J Biogeogr. 2013;40:1861-73.
84. Hampe A. Bioclimate envelope models: what they detect and what they hide. Global Ecol Biogeogr. 2004;13:469-71.
85. Hewitt GM. Genetic consequences of climatic oscillations in the Quaternary. Philos Trans R Soc B-Biol Sci. 2004;359:183-95.
86. Knowles LL, Richards CL. Importance of genetic drift during Pleistocene divergence as revealed by analyses of genomic variation. Mol Ecol. 2005;14:4023-32.
87. Murphy MA, Dezzani R, Pilliod DS, Storfer A. Landscape genetics of high mountain frog metapopulations. Mol Ecol. 2010;19:3634-49.
88. Benham PM, Witt CC. The dual role of Andean topography in primary divergence: functional and neutral variation among populations of the hummingbird, Metallura tyrianthina. BMC Evol Biol. 2016;16:22.
89. Reinhardt K, Kohler G, Maas S, Detzel P. Low dispersal ability and habitat specificity promote extinctions in rare but not in widespread species: the Orthoptera of Germany. Ecography. 2005;28:593-602.
90. San M, Gómez G, Van Dyck H. Ecotypic differentiation between urban and rural populations of the grasshopper Chorthippus brunneus relative to climate and habitat fragmentation. Oecologia. 2012;169:125-33.
91. Keller D, Holderegger R, van Strien MJ. Spatial scale affects landscape genetic analysis of a wetland grasshopper. Mol Ecol. 2013;22:2467-82.
92. Gauffre B, Mallez S, Chapuis MP, Leblois R, Litrico I, Delaunay S, et al. Spatial heterogeneity in landscape structure influences dispersal and genetic structure: empirical evidence from a grasshopper in an agricultural landscape. Mol Ecol. 2015;24:1713-28.
93. He Q, Edwards DL, Knowles LL. Integrative testing of how environments from the past to the present shape genetic structure across landscapes. Evolution. 2013;67:3386-402.
94. Laiolo P, Illera JC, Obeso JR. Local climate determines intra- and interspecific variation in sexual size dimorphism in mountain grasshopper communities. J Evol Biol. 2013;26:2171-83.
95. Roff DA, Mousseau T. The evolution of the phenotypic covariance matrix: evidence for selection and drift in Melanoplus. J Evol Biol. 2005;18:1104-14.
96. Grace T, Wisely SM, Brown SJ, Dowell FE, Joern A. Divergent host plant adaptation drives the evolution of sexual isolation in the grasshopper Hesperotettix viridis (Orthoptera: Acrididae) in the absence of reinforcement. Biol J Linn Soc. 2010;100:866-78.
97. Hernández-Teixidor D, López H, Nogales M, Emerson BC, Juan C, Oromí P. Genetic, morphological, and dietary changes associated with novel habitat colonisation in the Canary Island endemic grasshopper Acrostira bellamyi. Ecol Entomol. 2014;39:703-15.
98. Nosil P, Egan SP, Funk DJ. Heterogeneous genomic differentiation between walking-stick ecotypes: "Isolation by adaptation" and multiple roles for divergent selection. Evolution. 2008;62:316-36.
99. Funk DJ, Egan SP, Nosil P. Isolation by adaptation in Neochlamisus leaf beetles: host-related selection promotes neutral genomic divergence. Mol Ecol. 2011;20:4671-82.
100. Manthey JD, Moyle RG. Isolation by environment in White-breasted Nuthatches (Sitta carolinensis) of the Madrean archipelago sky islands: a landscape genomics approach. Mol Ecol. 2015;24:3628-38.
101. Sistrom M, Edwards DL, Donnellan S, Hutchinson M. Morphological differentiation correlates with ecological but not with genetic divergence in a Gehyra gecko. J Evol Biol. 2012;25:647-60.
102. Wang IJ, Summers K. Genetic structure is correlated with phenotypic divergence rather than geographic isolation in the highly polymorphic strawberry poison-dart frog. Mol Ecol. 2010;19:447-58.
103. Parks DH, Porter M, Churcher S, Wang S, Blouin C, Whalley J, et al. GENGIS: a geospatial information system for genomic data. Genome Res. 2009;19:1896-904.