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Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Latitudinal variation of genecological traits in native grasses of Patagonian rangelands

Paula E. Leva A C , Martín R. Aguiar A and Andrea C. Premoli B
+ Author Affiliations
- Author Affiliations

A Cátedra de Ecología-IFEVA, Facultad de Agronomía, Universidad de Buenos Aires/CONICET, Avenida San Martín 4453, (C1417DSE) Buenos Aires, Argentina.

B Laboratorio Ecotono, Universidad Nacional del Comahue/INIBIOMA CONICET, Quintral 1250, (8400) Bariloche – Río Negro, Argentina.

C Corresponding author. Email: pleva@agro.uba.ar

Australian Journal of Botany 61(6) 475-485 https://doi.org/10.1071/BT12249
Submitted: 24 July 2012  Accepted: 31 August 2013   Published: 1 November 2013

Abstract

Geographical variation in genetically based traits helps to elucidate the effect of distinct ecological and evolutionary processes on widespread plants. Whereas abundant information exists on genetic patterns of woody species in western humid Andes, such information is scarce for the neighbouring dry Patagonian steppe. We examined genecological traits of two native forage species vulnerable to overgrazing (Bromus pictus and Poa ligularis) in dry Occidental Phytogeographical District. We compared within-population genetic diversity and among-population (n = 6) divergence by using isozyme electrophoresis. We also cultivated plants under common garden to compare genetically based morphology (plant height, number of tillers by plant and weight per tiller). Analysis showed that 8 and 13 loci were polymorphic of 9 and 19 resolved loci in at least one population for Bromus and Poa, respectively. In general, plant traits decreased from north to south in both species. Genetic and quantitative results (FST/QST index) showed evidence of local adaptation in populations of both species. Genetic divergence among populations was significant. We detected two different geographical groups divided at the same latitude (42–43°S) in both species, supporting the hypothesis of a past vicariance event. Sustainable management of these forage species to cope with land-use and climate change will be enriched by the inclusion of genecological knowledge.


References

Aguiar MR, Román ME (2007) Restoring forage grass populations in arid Patagonian rangeland. In ‘Restoring natural capital: science, business and practice restoring natural capital’. (Eds J Aronson, S Milton, J Blignaut) pp. 112–121. (Island Press: Washington, DC)

Ares J (2007) Systems valuing of natural capital and investment in extensive pastoral systems: lessons from the Patagonian case. Ecological Economics 62, 162–173.
Systems valuing of natural capital and investment in extensive pastoral systems: lessons from the Patagonian case.Crossref | GoogleScholarGoogle Scholar |

Barrett SCH, Kohn JR (1991) Genetic and evolutionary consequences of small population size in plants: implications for conservation. In ‘Genetics and conservation of rare plants’. (Eds DA Falk, KE Holsinger) pp. 3–30. (Oxford University Press: Oxford, UK)

Cañón C, D’Elía G, Pardiñas UFJ, Lessa EP (2010) Phylogeography of Loxodontomys micropus with comments on the alpha taxonomy of Loxodontomys (Cricetidae: Sigmodontinae). Journal of Mammalogy 91, 1449–1458.
Phylogeography of Loxodontomys micropus with comments on the alpha taxonomy of Loxodontomys (Cricetidae: Sigmodontinae).Crossref | GoogleScholarGoogle Scholar |

Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annual Review of Plant Biology 58, 377–406.
Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnsVahsLs%3D&md5=53e21ac48d00e7ba3697d9b1e1a89c9fCAS | 17280525PubMed |

Cipriotti PA, Aguiar MR (2005) Effects of grazing on patch structure in a semi-arid two-phase vegetation mosaic. Journal of Vegetation Science 16, 57–66.
Effects of grazing on patch structure in a semi-arid two-phase vegetation mosaic.Crossref | GoogleScholarGoogle Scholar |

Comps B, Gömöry D, Letouzey J, Thiébaut B, Petit RJ (2001) Diverging trends between heterozygosity and allelic richness during postglacial colonization in the European Beech. Genetics 157, 389–397.

Cosacov A, Sérsic AN, Sosa V, Johnson LA, Cocucci AA (2010) Multiple periglacial refugia in the Patagonian steppe and post-glacial colonization of the Andes: the phylogeography of Calceolaria polyrhiza. Journal of Biogeography 37, 1463–1477.

Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends in Ecology & Evolution 15, 290–295.
Considering evolutionary processes in conservation biology.Crossref | GoogleScholarGoogle Scholar |

Ellstrand NC, Elam DR (1993) Population genetics consequences of small population size, implications for plant conservation. Annual Review of Ecology and Systematics 24, 217–242.
Population genetics consequences of small population size, implications for plant conservation.Crossref | GoogleScholarGoogle 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, 2611–2620.
Detecting the number of clusters of individuals using the software structure: a simulation study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvF2qtrg%3D&md5=bfa5ac1e764a9560d83fa60fc2fb6b62CAS | 15969739PubMed |

Fernández Pepi MG, Giussani LM, Morrone O (2008) Variabilidad morfológica de las especies del complejo Poa resinulosa (Poaceae) y su relación con las especies de la sección Dioicopoa. Darwiniana 46, 279–296.

García AM, Schrauf GE, González G, Poggio L, Naranjo CA, Dupal MP, Spangenberg GC, Forster JW (2009) Use of AFLP and RAPD molecular genetic markers and cytogenetic analysis to explore relationships among taxa of the Patagonian Bromus setifolius complex. Genetics and Molecular Biology 32, 312–319.
Use of AFLP and RAPD molecular genetic markers and cytogenetic analysis to explore relationships among taxa of the Patagonian Bromus setifolius complex.Crossref | GoogleScholarGoogle Scholar | 21637686PubMed |

Godt MJW, Hamrick JL (1998) Allozyme diversity in the grasses. In ‘Population biology of grasses’. (Ed. GP Cheplick) pp. 11–29. (Cambridge University Press: Cambridge, UK)

Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (v 2.9.3). Available at http://www.unil.ch/izea/softwares/fstat.html [Verified 21 October 2013]

Graff P, Aguiar MR, Chaneton EJ (2007) Shifts in positive and negative plant interactions along a grazing intensity gradient. Ecology 88, 188–199.
Shifts in positive and negative plant interactions along a grazing intensity gradient.Crossref | GoogleScholarGoogle Scholar | 17489467PubMed |

Hamrick JL, Godt MJW (1989) Allozyme diversity in plant species. In ‘Plant population genetics, breeding, and genetic resources’. (Eds AHD Brown, MT Clegg, AL Kahler, BS Weir) pp. 43–63. (Sinauer Associates: Sunderland, MA)

Hoisington D, Khairallah M, Reeves T, Ribaut JM, Skovmand B, Taba S, Warburton M (1999) Plant genetic resources: what can they contribute toward increased crop productivity? Proceedings of the National Academy of Sciences, USA 96, 5937–5943.
Plant genetic resources: what can they contribute toward increased crop productivity?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXksFKltbY%3D&md5=a40719bd8e466340f9fdfd514b47cc3fCAS |

Hunziker JH (1978) Cytogenetics and evolution of some species of Poa (Gramineae). In ‘Actas del III Congreso Latinoamericano de Genética’. (Eds ME Drets, N Brum-Zorrilla, GA Folle) pp. 144–148. (Asociación Latinoamericana de Genética: Montevideo, Uruguay)

Inda LA, Segarra-Moragues JG, Müller J, Peterson PM, Catalán P (2008) Dated historical biogeography of the temperate Loliinae (Poaceae, Pooideae) grasses in the northern and southern hemispheres. Molecular Phylogenetics and Evolution 46, 932–957.
Dated historical biogeography of the temperate Loliinae (Poaceae, Pooideae) grasses in the northern and southern hemispheres.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtlGrtro%3D&md5=63220c0b728b5cbd3ed9767e5d0425f2CAS | 18226932PubMed |

InfoStat (2008) ‘InfoStat versión 2008.’ (Grupo InfoStat, FCA, Universidad Nacional de Córdoba: Córdoba, Argentina)

Jakob S, Martinez-Meyer SE, Blattner FR (2009) Phylogeographic analyses and paleodistribution modeling indicate Pleistocene in situ survival of Hordeum species (Poaceae) in southern Patagonia without genetic or spatial restriction. Molecular Biology and Evolution 26, 907–923.
Phylogeographic analyses and paleodistribution modeling indicate Pleistocene in situ survival of Hordeum species (Poaceae) in southern Patagonia without genetic or spatial restriction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjt1Clurg%3D&md5=a41fde0d2a4c0be94e1e2f9bf0ae1d02CAS | 19168565PubMed |

Jonas CS, Geber MA (1999) Variation among populations of Clarkia unguiculata (Onagraceae) along altitudinal and latitudinal gradients. American Journal of Botany 86, 333–343.
Variation among populations of Clarkia unguiculata (Onagraceae) along altitudinal and latitudinal gradients.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MnhtVGruw%3D%3D&md5=8e1ec43b3e0fbcbefb453bc1e99b42d7CAS | 10077496PubMed |

Kellogg EA (2001) Evolutionary history of the grasses. Plant Physiology 125, 1198–1205.
Evolutionary history of the grasses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXitFWrt70%3D&md5=08c800fde97d32a3fa0fbef835cda850CAS | 11244101PubMed |

King JN, Dancik BP (1983) Inheritance and linkage of isozymes in white spruce (Picea glauca). Canadian Journal of Genetics and Cytology 5, 430–436.

Knight CA, Ackerly CC (2003) Evolution and plasticity of photosynthetic thermal tolerance, specific leaf area and leaf size: congeneric species from desert and coastal environments. New Phytologist 160, 337–347.
Evolution and plasticity of photosynthetic thermal tolerance, specific leaf area and leaf size: congeneric species from desert and coastal environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpt1Ogsbg%3D&md5=993dfbe9f6de8eb972ce368c53459956CAS |

Lessa EP, D’Elía G, Pardiñas UFJ (2010) Genetic footprints of late Quaternary climate change in the diversity of Patagonian–Fueguian rodents. Molecular Ecology 19, 3031–3037.
Genetic footprints of late Quaternary climate change in the diversity of Patagonian–Fueguian rodents.Crossref | GoogleScholarGoogle Scholar | 20618900PubMed |

Leva PE, Aguiar MR, Oesterheld M (2009) Underground ecology in a Patagonian steppe: root traits permit identification of graminoid species and classification into functional types. Journal of Arid Environments 73, 428–434.
Underground ecology in a Patagonian steppe: root traits permit identification of graminoid species and classification into functional types.Crossref | GoogleScholarGoogle Scholar |

Levin DA (1983) Polyploidy and novelty in flowering plants. American Naturalist 122, 1–25.
Polyploidy and novelty in flowering plants.Crossref | GoogleScholarGoogle Scholar |

Linhart YB, Premoli AC (1993) Comparison of the genetic variability in Aletes humilis, a rare plant species, and its common relative Aletes acaulis in Colorado. American Journal of Botany 80, 598–605.
Comparison of the genetic variability in Aletes humilis, a rare plant species, and its common relative Aletes acaulis in Colorado.Crossref | GoogleScholarGoogle Scholar |

Loveless MD, Hamrick JL (1984) Ecological determinants of genetic structure in plant populations. Annual Review of Ecology and Systematics 15, 65–95.
Ecological determinants of genetic structure in plant populations.Crossref | GoogleScholarGoogle Scholar |

Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Research 27, 209–220.

Marchelli P, Gallo LA (2006) Multiple ice-age refugia in a southern beech from southern South America as revealed by chloroplast DNA markers. Conservation Genetics 7, 591–603.
Multiple ice-age refugia in a southern beech from southern South America as revealed by chloroplast DNA markers.Crossref | GoogleScholarGoogle Scholar |

Martin G, Chapuis E, Goudet J (2008) Multivariate Q st–F st comparisons: a neutrality test for the evolution of the G matrix in structured populations. Genetics 180, 2135–2149.
Multivariate Q stF st comparisons: a neutrality test for the evolution of the G matrix in structured populations.Crossref | GoogleScholarGoogle Scholar | 18245845PubMed |

Mathiasen P, Premoli AC (2010) Out in the cold: genetic variation of Nothofagus pumilio (Nothofagaceae) provides evidence for latitudinally distinct evolutionary histories in austral South America. Molecular Ecology 19, 371–385.
Out in the cold: genetic variation of Nothofagus pumilio (Nothofagaceae) provides evidence for latitudinally distinct evolutionary histories in austral South America.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktlOntLY%3D&md5=3420b544a81a3d7d3856f842c07b3fdeCAS | 20002584PubMed |

Merilä J, Crnokrak P (2001) Comparison of genetic differentiation at marker loci and quantitative traits. Journal of Evolutionary Biology 14, 892–903.
Comparison of genetic differentiation at marker loci and quantitative traits.Crossref | GoogleScholarGoogle Scholar |

Mitton JB, Linhart YB, Sturgeon KB, Hamrick L (1979) Allozyme polymorphisms detected in mature needles of ponderosa pine. The Journal of Heredity 70, 86–89.

Moritz C (1994) Defining ‘evolutionary significant units’ for conservation. Trends in Ecology & Evolution 9, 373–375.
Defining ‘evolutionary significant units’ for conservation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFWhsA%3D%3D&md5=7c5afcd7e99030df5d1a10d86f323c2cCAS |

Naranjo CA, Arias FH, Gil FE, Soriano A (1990) Bromus pictus of the Bromus setifolius complex (section Pnigma): numerical taxonomy and chromosome evidence for species rank. Canadian Journal of Botany 68, 2493–2500.

Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89, 583–590.

Nei M, Maruyama T, Charaborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29, 1–10.
The bottleneck effect and genetic variability in populations.Crossref | GoogleScholarGoogle Scholar |

Noss RF (1990) Indicators for monitoring biodiversity: a hierarchical approach. Conservation Biology 4, 355–364.
Indicators for monitoring biodiversity: a hierarchical approach.Crossref | GoogleScholarGoogle Scholar |

Oñatibia GR, Aguiar MR, Cipriotti PA, Troiano F (2010) Individual plant and population biomass of dominant shrubs in Patagonian grazed fields. Ecología Austral 20, 269–270.

Paruelo JM, Beltrán A, Jobbágy EG, Sala OE, Golluscio RA (1998) The climate of Patagonia: general patterns and controls on biotic processes. Ecología Austral 8, 85–101.

Pastorino MJ, Ghirardi S, Grosfeld J, Gallo LA, Puntieri JG (2010) Genetic variation in architectural seedling traits of Patagonian cypress natural populations from the extremes of a precipitation range. Annals of Forest Science 67, 508–518.
Genetic variation in architectural seedling traits of Patagonian cypress natural populations from the extremes of a precipitation range.Crossref | GoogleScholarGoogle Scholar |

Peakall R, Smouse PE (2006) Program note Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.
Program note Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research.Crossref | GoogleScholarGoogle Scholar |

Poorter H, Remkes C (1990) Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate. Oecologia 83, 553–559.
Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate.Crossref | GoogleScholarGoogle Scholar |

Premoli AC (1997) Genetic variation in a geographically restricted and two widespread species of South American Nothofagus. Journal of Biogeography 24, 883–892.
Genetic variation in a geographically restricted and two widespread species of South American Nothofagus.Crossref | GoogleScholarGoogle Scholar |

Premoli AC (1998) The use of genetic markers to conserve endangered species and to design protected areas of more widespread species. In ‘Proceedings of an international workshop: recent advances in biotechnology for tree conservation and management’. (Ed. International Foundation for Science) pp. 157–171. (Universidade Federal de Santa Catarina, Florianópolis: Santa Catarina, Brasil)

Premoli AC, Brewer CA (2007) Environmental v. genetically driven variation in ecophysiological traits of Nothofagus pumilio from contrasting elevations. Australian Journal of Botany 55, 585–591.
Environmental v. genetically driven variation in ecophysiological traits of Nothofagus pumilio from contrasting elevations.Crossref | GoogleScholarGoogle Scholar |

Premoli AC, Kitzberger T (2005) Regeneration mode affects spatial genetic structure of Nothofagus dombeyi forests in northwestern Patagonia. Molecular Ecology 14, 2319–2329.
Regeneration mode affects spatial genetic structure of Nothofagus dombeyi forests in northwestern Patagonia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvF2qsLo%3D&md5=695beaee9a55b507ca525706f8904a15CAS | 15969717PubMed |

Premoli AC, Kitzberger T, Veblen TT (2000) Isozyme variation and recent biogeographical history of the long-lived conifer Fitzroya cupressoides. Journal of Biogeography 27, 251–260.
Isozyme variation and recent biogeographical history of the long-lived conifer Fitzroya cupressoides.Crossref | GoogleScholarGoogle Scholar |

Premoli AC, Raffaele E, Mathiasen P (2007) Contrasting elevations maintain heritable morphological and phenological differences in Nothofagus pumilio. Austral Ecology 32, 515–523.
Contrasting elevations maintain heritable morphological and phenological differences in Nothofagus pumilio.Crossref | GoogleScholarGoogle Scholar |

Premoli AC, Mathiasen P, Kitzberger T (2010) Southern-most Nothofagus trees enduring ice ages: genetic evidence and ecological niche retrodiction reveal high latitude (54°S) glacial refugia. Palaeogeography, Palaeoclimatology, Palaeoecology 298, 247–256.
Southern-most Nothofagus trees enduring ice ages: genetic evidence and ecological niche retrodiction reveal high latitude (54°S) glacial refugia.Crossref | GoogleScholarGoogle Scholar |

Premoli AC, Mathiasen P, Acosta CM, Ramos VA (2012) Phylogeographically concordant chloroplast DNA divergence in sympatric Nothofagus s.s. How deep can it be? New Phytologist 193, 261–275.
Phylogeographically concordant chloroplast DNA divergence in sympatric Nothofagus s.s. How deep can it be?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XitVKgt7k%3D&md5=aed061e1260ee577ef45b8ae6a471dceCAS | 21883239PubMed |

Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.

Quiroga MP, Premoli AC (2010) Genetic structure of Podocarpus nubigena (Podocarpaceae) provides evidence of Quaternary and ancient historical events. Palaeogeography, Palaeoclimatology, Palaeoecology 285, 186–193.
Genetic structure of Podocarpus nubigena (Podocarpaceae) provides evidence of Quaternary and ancient historical events.Crossref | GoogleScholarGoogle Scholar |

Rabassa J (2008) Late Cenozoic glaciations in Patagonia and Tierra del Fuego. In ‘The Late Cenozoic of Patagonia and Tierra del Fuego’. (Ed. J Rabassa) pp. 151–204. (Elsevier: Oxford, UK)

Ranker TA, Haufler CH, Soltis PS, Soltis DE (1989) Genetic evidence for allopolyploidy in the neotropical fern Hemionitis (Adiantaceae) and the reconstruction of an ancestral genome. Systematic Botany 14, 439–447.
Genetic evidence for allopolyploidy in the neotropical fern Hemionitis (Adiantaceae) and the reconstruction of an ancestral genome.Crossref | GoogleScholarGoogle Scholar |

Schemske DW, Husband BC, Ruckelshaus MH, Goodwillie C, Parker IM, Bishop JG (1994) Evaluating approaches to the conservation of rare and endangered plants. Ecology 75, 584–606.
Evaluating approaches to the conservation of rare and endangered plants.Crossref | GoogleScholarGoogle Scholar |

Sede SM, Nicola MV, Pozner R, Johnson LA (2012) Phylogeography and palaeodistribution modelling in the Patagonian steppe: the case of Mulinum spinosum (Apiaceae). Journal of Biogeography 39, 1041–1057.
Phylogeography and palaeodistribution modelling in the Patagonian steppe: the case of Mulinum spinosum (Apiaceae).Crossref | GoogleScholarGoogle Scholar |

Sérsic AN Cosacov A Cocucci1 AA Johnson LA Pozner R Avila LJ Sites JW Jr Morando M 2011 Emerging phylogeographical patterns of plants and terrestrial vertebrates from Patagonia. Biological Journal of the Linnean Society 103 475 494

Soltis DE, Rieseberg LH (1986) Autopolyploidy in Tolmiea menziesii (Saxifragaceae): evidence from enzyme electrophoresis. American Journal of Botany 73, 310–318.
Autopolyploidy in Tolmiea menziesii (Saxifragaceae): evidence from enzyme electrophoresis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XktVelur4%3D&md5=8d65fc36dfa76fbe558c5e4d4c6d3fa6CAS |

Souto CP, Premoli AC, Reich PB (2009) Complex bioclimatic and soil gradients shape leaf trait variation in Embothrium coccineum (Proteaceae) among austral forests in Patagonia. Revista Chilena de Historia Natural 82, 209–222.
Complex bioclimatic and soil gradients shape leaf trait variation in Embothrium coccineum (Proteaceae) among austral forests in Patagonia.Crossref | GoogleScholarGoogle Scholar |

Strömberg CAE (2011) Evolution of grasses and grassland ecosystems. Annual Review of Earth and Planetary Sciences 39, 517–544.
Evolution of grasses and grassland ecosystems.Crossref | GoogleScholarGoogle Scholar |

Tremetsberger K, Urtubey E, Terrab A, Baeza CM, Ortiz MA, Talavera M, König C, Temsch EM, Kohl G, Talavera S, Stuessy TF (2009) Pleistocene refugia and polytopic replacement of diploids by tetraploids in the Patagonian and Subantarctic plant Hypochaeris incana (Asteraceae, Cichorieae). Molecular Ecology 18, 3668–3682.
Pleistocene refugia and polytopic replacement of diploids by tetraploids in the Patagonian and Subantarctic plant Hypochaeris incana (Asteraceae, Cichorieae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1WhtrnF&md5=f1a9748fc1ea3c8a975b385792432131CAS | 19674310PubMed |

Vidal-Russell R, Souto CP, Premoli AC (2011) Multiple Pleistocene refugia in the widespread Patagonian tree Embothrium coccineum (Proteaceae). Australian Journal of Botany 59, 299–314.

Villagrán C, Hinojosa LF (2005) Esquema biogeográfico de Chile. In ‘Regionalización biogeográfica en Iberoámeríca y tópicos afines’. (Eds J Llorente Bousquets, JJ Morrone) pp. 551–577. (Ediciones de la Universidad Nacional Autónoma de México: D.F.)

Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.
Estimating F-statistics for the analysis of population structure.Crossref | GoogleScholarGoogle Scholar |

Wright S (1965) The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19, 395–420.
The interpretation of population structure by F-statistics with special regard to systems of mating.Crossref | GoogleScholarGoogle Scholar |