Genetic variation in the widespread Embothrium coccineum (Proteaceae) endemic to Patagonia: effects of phylogeny and historical events
Cintia P. Souto A B and Andrea C. Premoli AA Laboratorio Ecotono, Universidad Nacional del Comahue, Quintral 1250, Bariloche (8400), Río Negro, Argentina.
B Corresponding author. Email: csouto@crub.uncoma.edu.ar
Australian Journal of Botany 55(8) 809-817 https://doi.org/10.1071/BT06183
Submitted: 30 August 2006 Accepted: 27 August 2007 Published: 14 December 2007
Abstract
Allozyme electrophoresis was used to measure and compare, with other members of the Proteaceae, levels and distribution of genetic diversity in Embothrium coccineum J.R.Forst., a widespread outcrossing species endemic of Andean Patagonian forests. We analysed variation at the species level by sampling 34 populations along its entire range of ~20° latitude. We tested the hypothesis of multiple Pleistocene refugia by phylogeographic methods. We resolved 16 isozyme loci assayed in 934 adult trees. At the species level, total genetic diversity (HT = 0.220) was similar to that of other outcrossed and widespread plant species. Genetic parameters (NA, PSS, HE) were not statistically different from other outcrossed but mostly range-restricted Proteaceae, reflecting a strong phylogenetic imprinting for species sharing life-history traits. Populations are genetically divergent among each other (FST = 0.202). The low correlation between geographic and genetic distances suggests separate histories, i.e. multiple glacial refugia for the cold-tolerant E. coccineum. Phylogeographic trees produced different topologies, although maximum likelihood and parsimony trees shared some elements. Both trees suggest a northern and central clade, and then a separate southern clade. Current processes such as gene flow and selection confound the historic signal. These results seem in contrast to many of the northern hemisphere post-glacial phylogeographic reconstructions which show clear historical tracks of northern range expansion from southern refugia. The present study highlights the importance of phylogenetic imprinting, life-history traits and historical events driving genetic diversity patterns in this widespread Proteaceae from southern South America.
Acknowledgements
Field work was supported by a Field Grant from the British Genetic Society. This research was also funded by the European Commission under Framework IV of DGXII, as part of the BIOCORES project (PL ICA4–2000–10029). We thank National Park authorities of Argentina and Chile for logistical support and for facilitating access to protected areas. We thank A. Boi, F. Boi, S. Boi, P. Quiroga and A. Rovere for help during the field work. P. Mathiasen provided valuable assistance in the laboratory. A. Ruggiero and R. Vidal helped with figures. E. Gonzales and M. Rossetto made helpful suggestions on early versions of this manuscript. We also thank two anonymous reviewers for their suggestions that greatly improved the clarity and the science of our manuscript. C.P.S. and A.C.P. are members of CONICET.
Ayre DJ,
Whelan RJ, Reid A
(1994) Unexpectedly high levels of selfing in the Australian shrub Grevillea barklyana (Proteaceae). Heredity 72, 168–174.
Berlocher SH, Swofford DL
(1997) Searching for phylogenetic trees under the frequency parsimony criterion: an approximation using generalized parsimony. Systematic Biology 46, 211–215.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Broadhurst LM, Coates DJ
(2004) Genetic divergence among and diversity within two rare Banksia species and their common close relative in the subgenus Isostylis R.Br. (Proteaceae). Journal of Conservation Genetics 5, 837–846.
| Crossref |
Cadzow B, Carthew SM
(2000) Breeding system and fruit development in Persoonia juniperina (Proteaceae). Cunninghamia 6, 941–950.
Carthew SM
(1993) Population genetic structure of Banksia spinulosa. Heredity 70, 566–573.
Cavalli-Sforza LL, Edwards AWF
(1967) Phylogenetic analysis: models and estimation procedures. Evolution 21, 550–570.
| Crossref | GoogleScholarGoogle Scholar |
Coates DJ, Sokolowski RES
(1992) The mating system and patterns of genetic variation in Banksia cuneata AS George (Proteaceae). Heredity 69, 11–20.
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.
| PubMed |
Cwynar LC, MacDonald GM
(1987) Geographical variation of lodgepole pine in relation to population history. American Naturalist 129, 463–469.
| Crossref | GoogleScholarGoogle Scholar |
Devoto M,
Montaldo NH, Medan D
(2006) Mixed hummingbird: long-proboscid-fly pollination in ‘ornithophilous’ Embothrium coccineum (Proteaceae) along a rainfall gradient in Patagonia, Argentina. Austral Ecology 31, 512–519.
| Crossref | GoogleScholarGoogle Scholar |
Dimitri MJ, Correa Luna H
(1967) La flora Andino Patagónica. Estudio fitosociológico de una comunidad edáfica entre Puerto Blest y Laguna Frías, del Parque Nacional Nahuel Huapi. Anales de Parques Nacionales 11, 4–42.
Dumolin-Lapegue S,
Demesure B,
Fineschi S,
Le Corre V, Petit RJ
(1997) Phylogeographic structure of white oaks throughout the European continent. Genetics 146, 1475–1487.
| PubMed |
Felsenstein J
(1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. Journal of Molecular Evolution 17, 368–376.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Goldingay RL, Carthew SM
(1998) Breeding and mating systems of Australian Proteaceae. Australian Journal of Botany 46, 421–437.
| Crossref | GoogleScholarGoogle Scholar |
Hamrick JL,
Godt MJW, Sherman-Broyles SL
(1992) Factors influencing levels of genetic diversity in woody plant species. New Forests 6, 95–124.
| Crossref | GoogleScholarGoogle Scholar |
Harwood CE,
Moran GF, Bell JC
(1997) Genetic differentiaion in natural populations of Grevillea robusta. Australian Journal of Botony 46, 669–678.
| Crossref |
Heuertz M,
Fineschi S,
Anzidei M,
Pastorelli R,
Salvini D,
Paule L,
Frascaria-Lacoste N,
Hardy OJ,
Vekemans X, Vendramin GG
(2004) Chloroplast DNA variation and postglacial recolonization of common ash (Fraxinus excelsior L.) in Europe. Molecular Ecology 13, 3437–3452.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Heusser CJ
(1984) Late-glacial–Holocene climate of Lake District of Chile. Quaternary Research 22, 77–90.
| Crossref | GoogleScholarGoogle Scholar |
Heusser CJ,
Lowell TV,
Heusser LE,
Hauser A, Björn G
(1996) Full-glacial–late-glacial paleoclimate of the southern Andes: evidence from pollen, beetle and glacial records. Journal of Quaternary Science 11, 173–184.
| Crossref | GoogleScholarGoogle Scholar |
Hewitt GM
(2000) The genetic legacy of the Quaternary ice ages. Nature 405, 907–913.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hoebee SE, Young AG
(2001) Low neighbourhood size and high interpopulation differentiation in the endangered shrub Grevillea iaspicula McGill (Proteaceae). Heredity 86, 489–496.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Krauss SL
(1997) Low genetic diversity in Persoonia mollis (Proteaceae), a fire-sensitive shrub occurring in a fire-prone habitat. Heredity 78, 41–49.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Krauss SL
(1998) A phylogeographic analysis of allozyme variation among populations of Persoonia mollis (Proteaceae). Australian Journal of Botany 46, 571–582.
| Crossref | GoogleScholarGoogle Scholar |
Lewis PO, Crawford DJ
(1995) Pleistocene refugium endemics exhibit greater allozymic diversity than widespread congeners in the genus Polygonella (Polygonaceae). American Journal of Botany 82, 141–149.
| Crossref | GoogleScholarGoogle Scholar |
Lynch AJJ,
Barnes RW,
Cambacedes AJ, Vaillancourt RE
(1998) Genetic evidence that Lomatia tasmanica (Proteaceae) is an ancient clone. Australian Journal of Botony 46, 25–33.
| Crossref |
Mantel N
(1967) The detection of disease clustering and a generalized regression approach. Cancer Research 27, 209–220.
| PubMed |
Markgraf V
(1993) Paleoenvironments and paleoclimates in Tierra del Fuego and southernmost Patagonia, South America. Paleogeography, Paleoclimatology, Paleoecology 102, 53–68.
| Crossref | GoogleScholarGoogle Scholar |
Markgraf V,
McGlone M, Hope G
(1995) Neogene paleoenvironmental and paleoclimatic change in southern temperate ecosystems—a southern perspective. Trends in Ecology & Evolution 10, 143–147.
| Crossref | GoogleScholarGoogle Scholar |
Mitton JB,
Linhart YB,
Sturgeon KB, Hamrick JL
(1979) Allozyme polymorphisms detected in mature needle tissue of ponderosa pine. Journal of Heredity 70, 86–89.
Nei M
(1973) Analysis of gene diversity in subdivided populations. Proceedings of the National Academy of Sciences, USA 70, 3321–3323.
| Crossref | GoogleScholarGoogle Scholar |
O’Malley DM,
Allendorf FW, Blake GM
(1979) Inheritance of isozyme variation and heterozygosity in ponderosa pine. Biochemical Genetics 17, 233–250.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Petit RJ,
Brewer S,
Bordács S,
Burg K,
Cheddadi R,
Coart E,
Cottrell J,
Csaikl UM,
van Dam B,
Deans JD,
Espinel S,
Fineschi S,
Finkeldey R,
Glaz I,
Goicoechea PG,
Jensen JS,
König AO,
Lowe AJ,
Madsen SF,
Mátyás G,
Munro RC,
Popescu F,
Slade D,
Tabbener H,
de Vries SGM,
Ziegenhagen B,
de Beaulieu J-L, Kremer A
(2002a) Identification of refugia and post-glacial colonisation routes of European white oaks based on chloroplast DNA and fossil pollen evidence. Forest Ecology and Management 156, 49–74.
| Crossref | GoogleScholarGoogle Scholar |
Petit RJ,
Csaikl UM,
Bordács S,
Burg K,
Coart E,
Cottrell J,
van Dam BC,
Deans JD,
Dumolin-Lapegue S,
Fineschi S,
Finkeldey R,
Gillies A,
Glaz I,
Goicoechea PG,
Jensen JS,
König AO,
Lowe AJ,
Madsen SF,
Mátyás G,
Munro RC,
Pemonge M-H,
Popescu F,
Slade D,
Tabbener H,
Taurchini D,
de Vries SGM,
Ziegenhagen B, Kremer A
(2002b) Chloroplast DNA variation in European white oaks. Phylogeography and patterns of diversity based on data from over 2600 populations. Forest Ecology and Management 156, 5–26.
| Crossref | GoogleScholarGoogle Scholar |
Petit RJ, Kremer DB
(1993) Geographical structure of chloroplast DNA polymorphisms in European oaks. Theoretical and Applied Genetics 87, 122–128.
| Crossref | GoogleScholarGoogle Scholar |
Poulik MD
(1957) Starch gel electrophoresis in a discontinuous system of buffers. Nature 180, 1477–1479.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
Premoli AC,
Souto CP,
Allnutt TR, Newtons AC
(2001) Effects of population disjunction on isozyme variation in the widespread Pilgerodendron uviferum. Heredity 87, 337–343.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rossetto M,
Weaver PK, Dixon KW
(1995) Use of RAPD analysis in devising conservation strategies for the rare and endangered Grevillea scapigera (Proteaceae). Molecular Ecology 4, 321–329.
| PubMed |
Rovere AE, Premoli AC
(2005) Dispersión asimétrica de semillas de Embothrium coccineum (Proteaceae) en el bosque templado de Chiloé, Chile. Ecología Austral 15, 1–7.
Rovere AE,
Smith-Ramírez C,
Armesto JJ, Premoli AC
(2006) Sistema reproductivo de Embothrium coccineum (Proteaceae). Revista Chilena de Historia Natural 79, 225–232.
Smith-Ramírez C, Armesto JJ
(2003) Foraging behaviour of bird pollinators on Embothrium coccineum (Proteaceae) trees in forest fragments and pastures in southern Chile. Austral Ecology 28, 53–60.
| Crossref | GoogleScholarGoogle Scholar |
Soltis DE,
Haufler CH,
Darrow DC, Gastony GJ
(1983) Starch gel electrophoresis of ferns: a compilation of grinding buffers, gel and electrode buffers, and staining schedules. American Fern Journal 73, 9–27.
| Crossref | GoogleScholarGoogle Scholar |
Starr GJ, Carthew SM
(1998) Genetic differentiation in isolated populations of Hakea carinata (Proteaceae). Australian Journal of Botany 46, 671–682.
| Crossref | GoogleScholarGoogle Scholar |
Steubing L,
Alberdi M, Wenzel H
(1983) Seasonal changes of cold resistance of Proteaceae of the south Chilean laurel forest. Vegetatio 52, 35–44.
Swofford DL, Berlocher SH
(1987) Inferring evolutionary trees from gene frequency data under the principal of maximum parsimony. Systematic Zoology 36, 293–325.
| Crossref | GoogleScholarGoogle Scholar |
Villagrán C
(1991) Historia de los bosques templados del sur de Chile durante el Tardiglacial y Postglacial. Revista Chilena de Historia Natural 64, 447–460.
Villagrán C,
Armesto JJ, Leiva R
(1986) Recolonización postglacial de Chiloé insular: evidencias basadas en la distribución geográfica y los modos de dispersión de la flora. Revista Chilena de Historia Natural 59, 19–39.
Wiens JJ
(1995) Polymorphic characters in phylogenetic systematics. Systematic Biology 44, 482–500.
| Crossref | GoogleScholarGoogle Scholar |
Wiens JJ
(2000) Reconstructing phylogenies from allozyme data: testing method performance with congruence. Biological Journal of the Linnean Society 70, 613–632.
| 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.
| Crossref | GoogleScholarGoogle Scholar |
