Nothofagus trees show genotype difference that influence infection by mistletoes, Misodendraceae
Romina Vidal-Russell A B and Andrea C. Premoli A
+ Author Affiliations
- Author Affiliations
A Laboratorio Ecotono, INIBIOMA (CONICET-Universidad Nacional del Comahue) Quintral 1250 (8400) Bariloche, Rio Negro, Argentina.
B Corresponding author. Email: vidalrussell@comahue-conicet.gob.ar
Australian Journal of Botany 63(6) 541-548 https://doi.org/10.1071/BT14306
Submitted: 12 February 2014 Accepted: 26 June 2015 Published: 3 August 2015
Abstract
Nothofagus trees host Misodendrum, an endemic mistletoe of the subantarctic forests of Chile and Argentina. Differences in the infection intensity on a given host and patches of infected trees are observed within the forest. We used allozymes to test for genetic differences between uninfected and infected Nothofagus trees (Nothofagus antarctica (G. Forst.) Oerst.) by two species of Misodendrum (Misodendrum linearifolium DC. and Misodendrum punctulatum DC.) at three sites. Non-metric multidimensional scaling ordination was performed using the presence of each of 26 total alleles in 166 trees of N. antarctica (89 uninfected and 77 infected). Sites with higher degrees of infection by M. punctulatum can be distinguished in the ordination. The number of infections per tree has a significant correlation with the ordination axis. ANOSIM analysis showed significant differences between infected and uninfected trees when they were infected by M. punctulatum but not by M. linearifolium. Differences between sites were also found, but the two sites with higher degrees of infection by M. punctulatum did not differ from each other. The intrapopulation genetic structure of N. antarctica could be maintained by the mistletoe Misodendrum through host selection.
Additional keywords: isozyme, Misodendrum linearifolium, Misodendrum punctulatum, Nothofagus antarctica, parasitic plants, Patagonia, resistance.
References
Altizer S, Pedersen AB (2008) Host–pathogen evolution, biodiversity and disease risks for natural populations. In ‘Conservation biology: evolution in action’. (Eds SP Carroll, CW Fox) pp. 259–277. (Oxford University Press: New York)Amico GC, Vidal-Russell R, Nickrent DL (2007) Phylogenetic relationships and ecological speciation in the mistletoe Tristerix (Loranthaceae): The influence of pollinators, dispersers, and hosts. American Journal of Botany 94, 558–567.
| Phylogenetic relationships and ecological speciation in the mistletoe Tristerix (Loranthaceae): The influence of pollinators, dispersers, and hosts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlt1Ggs7s%3D&md5=7721d3df2e11ae30a7f1e1be6ed83f99CAS | 21636426PubMed |
Arnaud M-C, Véronési C, Thalouarn P (1999) Physiology and histology of resistance to Striga hermonthica in Sorghum bicolor var. Framida. Functional Plant Biology 26, 63–70.
Aukema JE (2003) Vectors, viscin, and Viscaceae: mistletoes as parasites, mutualists, and resources. Frontiers in Ecology and the Environment 1, 212–219.
| Vectors, viscin, and Viscaceae: mistletoes as parasites, mutualists, and resources.Crossref | GoogleScholarGoogle Scholar |
Aukema JE, Martínez del Rio C (2002) Where does a fruit-eating bird deposit mistletoe seeds? Seed deposition patterns and an experiment. Ecology 83, 3489–3496.
| Where does a fruit-eating bird deposit mistletoe seeds? Seed deposition patterns and an experiment.Crossref | GoogleScholarGoogle Scholar |
Bach CE, Kelly D, Hazlett BA (2005) Forest edges benefit adults, but not seedlings, of the mistletoe Alepis flavida (Loranthaceae). Journal of Ecology 93, 79–86.
| Forest edges benefit adults, but not seedlings, of the mistletoe Alepis flavida (Loranthaceae).Crossref | GoogleScholarGoogle Scholar |
Cameron DD, Hwangbo J-K, Keith AM, Geniez J-M, Kraushaar D, Rowntree J, Seel WE (2005) Interactions between the hemiparasitic angiosperm Rhinanthus minor and its hosts: from the cell to the ecosystem. Folia Geobotanica 40, 217–229.
| Interactions between the hemiparasitic angiosperm Rhinanthus minor and its hosts: from the cell to the ecosystem.Crossref | GoogleScholarGoogle Scholar |
Cameron DD, Coats AM, Seel WE (2006) Differential resistance among host and non-host species underlies the variable success of the hemi-parasitic plant Rhinanthus minor. Annals of Botany 98, 1289–1299.
| Differential resistance among host and non-host species underlies the variable success of the hemi-parasitic plant Rhinanthus minor.Crossref | GoogleScholarGoogle Scholar | 17008350PubMed |
Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18, 117–143.
| Non-parametric multivariate analyses of changes in community structure.Crossref | GoogleScholarGoogle Scholar |
Clay K, Dement D, Rejmanek M (1985) Experimental evidence for host races in mistletoe (Phoradendron tomentosum). American Journal of Botany 72, 1225–1231.
| Experimental evidence for host races in mistletoe (Phoradendron tomentosum).Crossref | GoogleScholarGoogle Scholar |
Combes C (2001) ‘Parasitism: the ecology and evolution of intimate interactions.’ (University of Chicago Press: Chicago, IL, USA)
Gandon S, Michalakis Y (2002) Local adaptation, evolutionary potential and host–parasite coevolution: interactions between migration, mutation, population size and generation time. Journal of Evolutionary Biology 15, 451–462.
| Local adaptation, evolutionary potential and host–parasite coevolution: interactions between migration, mutation, population size and generation time.Crossref | GoogleScholarGoogle Scholar |
Ganz HH, Ebert D (2010) Benefits of host genetic diversity for resistance to infection depend on parasite diversity. Ecology 91, 1263–1268.
| Benefits of host genetic diversity for resistance to infection depend on parasite diversity.Crossref | GoogleScholarGoogle Scholar | 20503859PubMed |
García D, Rodríguez‐Cabal MA, Amico GC (2009) Seed dispersal by a frugivorous marsupial shapes the spatial scale of a mistletoe population. Journal of Ecology 97, 217–229.
| Seed dispersal by a frugivorous marsupial shapes the spatial scale of a mistletoe population.Crossref | GoogleScholarGoogle Scholar |
Geils BW, Cibrián Tovar J, Moody B (2002) Mistletoes of North American conifers. (General Technical Report-Rocky Mountain Research Station, USDA Forest Service: Fort Collins, CO)
Glazner JT, Devlin B, Ellstrand NC (1988) Biochemical and morphological evidence for host race evolution in desert mistletoe, Phoradendron californicum (Viscaceae). Plant Systematics and Evolution 161, 13–21.
| Biochemical and morphological evidence for host race evolution in desert mistletoe, Phoradendron californicum (Viscaceae).Crossref | GoogleScholarGoogle Scholar |
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (Ver. 2.9. 3). Available at http://www.unil.ch/izea/softwares/fstat.htm [Verified 9 July 2015]
Hawksworth FG, Wiens D (1996) ‘Dwarf mistletoes: biology, pathology and systematics.’ (USDA Forest Service: Washington DC)
Joshi J, Matthies D, Schmid B (2000) Root hemiparasites and plant diversity in experimental grassland communities. Journal of Ecology 88, 634–644.
| Root hemiparasites and plant diversity in experimental grassland communities.Crossref | GoogleScholarGoogle Scholar |
Kaltz O, Shykoff JA (1998) Local adaptation in host–parasite systems. Heredity 81, 361–370.
| Local adaptation in host–parasite systems.Crossref | GoogleScholarGoogle Scholar |
Kelly CK, Venable DL, Zimmerer K (1988) Host specialization in Cuscuta costaricensis: an assessment of host use relative to host availability. Oikos 53, 315–320.
| Host specialization in Cuscuta costaricensis: an assessment of host use relative to host availability.Crossref | GoogleScholarGoogle Scholar |
Koskela T, Salonen V, Mutikainen P (2000) Local adaptation of a holoparasitic plant, Cuscuta europaea: variation among populations. Journal of Evolutionary Biology 13, 749–755.
| Local adaptation of a holoparasitic plant, Cuscuta europaea: variation among populations.Crossref | GoogleScholarGoogle Scholar |
Koskela T, Puustinen S, Salonen V, Mutikainen P (2002) Resistance and tolerance in a host plant–holoparasitic plant interaction: genetic variation and costs. Evolution 56, 899–908.
Kruskal JB (1964a) Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29, 1–27.
| Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis.Crossref | GoogleScholarGoogle Scholar |
Kruskal JB (1964b) Nonmetric multidimensional scaling: a numerical method. Psychometrika 29, 115–129.
| Nonmetric multidimensional scaling: a numerical method.Crossref | GoogleScholarGoogle Scholar |
Kuijt J (1969) ‘The biology of parasitic flowering plants.’ (University of California Press: Berkeley, CA, USA)
Laine AL (2005) Spatial scale of local adaptation in a plant–pathogen metapopulation. Journal of Evolutionary Biology 18, 930–938.
| Spatial scale of local adaptation in a plant–pathogen metapopulation.Crossref | GoogleScholarGoogle Scholar | 16033565PubMed |
Linhart YB (1989) Interactions between genetic and ecological patchiness in forest trees and their dependent species. In ‘Evolutionary ecology of plants’. pp. 393–430. (Westview Press: Boulder, CO)
Linhart YB, Grant MC (1996) Evolutionary significance of local genetic differentiation in plants. Annual Review of Ecology and Systematics 27, 237–277.
| Evolutionary significance of local genetic differentiation in plants.Crossref | GoogleScholarGoogle Scholar |
Linhart YB, Snyder MA, Gibson JP (1994) Differential host utilization by two parasites in a population of ponderosa pine. Oecologia 98, 117–120.
| Differential host utilization by two parasites in a population of ponderosa pine.Crossref | GoogleScholarGoogle Scholar |
Lively CM, Dybdahl MF (2000) Parasite adaptation to locally common host genotypes. Nature 405, 679–681.
| Parasite adaptation to locally common host genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktlCgu7w%3D&md5=eafa7a360526bab59504ea1b22bef2aeCAS | 10864323PubMed |
Martinez del Rio C, Hourdequin M, Silva A, Medel R (1995) The influence of cactus size and previous infection on bird deposition of mistletoe seeds. Australian Journal of Ecology 20, 571–576.
| The influence of cactus size and previous infection on bird deposition of mistletoe seeds.Crossref | GoogleScholarGoogle Scholar |
McQueen DR (1976) The ecology of Nothofagus and associated vegetation in South America. Tuatara 22, 38–68.
Medel R, Vergara E, Silva A, Kalin-Arroyo M (2004) Effects of vector behavior and host resistance on mistletoe aggregation. Ecology 85, 120–126.
| Effects of vector behavior and host resistance on mistletoe aggregation.Crossref | GoogleScholarGoogle Scholar |
Minchin PR (2004) ‘Database for ecological community data (DECODA). Ver. 3.00 b31.’ (University of Melbourne: Melbourne)
Mitton JB, Linhart YB, Sturgeon KB, Hamrick JL (1979) Allozyme polymorphisms detected in mature needle tissue of ponderosa pine. The Journal of Heredity 70, 86–89.
Mutikainen P, Koskela T (2002) Population structure of a parasitic plant and its perennial host. Heredity 89, 318–324.
| Population structure of a parasitic plant and its perennial host.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38votVSmsA%3D%3D&md5=15365ebd1d3b393eb94449bbc5cb6b2dCAS | 12242649PubMed |
Mutikainen P, Salonen V, Puustinen S, Koskela T (2000) Local adaptation, resistance, and virulence in a hemiparasitic plant–host plant interaction. Evolution 54, 433–440.
Norton DA, Smith MS (1999) Why might roadside mulgas be better mistletoe hosts? Australian Journal of Ecology 24, 193–198.
| Why might roadside mulgas be better mistletoe hosts?Crossref | GoogleScholarGoogle Scholar |
Núñez-Farfán J, Fornoni J, Valverde PL (2007) The evolution of resistance and tolerance to herbivores. Annual Review of Ecology Evolution and Systematics 38, 541–566.
| The evolution of resistance and tolerance to herbivores.Crossref | GoogleScholarGoogle Scholar |
Orfila EN (1978) ‘Misodendraceae de la Argentina y Chile.’ (Fundación Elías y Ethel Malamud: Buenos Aires)
Overton JM (1994) Dispersal and infection in mistletoe metapopulations. Journal of Ecology 82, 711–723.
| Dispersal and infection in mistletoe metapopulations.Crossref | GoogleScholarGoogle Scholar |
Parker C, Riches CR (1993) ‘Parasitic weeds of the world: biology and control.’ (CAB International Center for Agricultural Biosciences: Oxon, UK)
Premoli AC (1991) Morfología y capacidad germinativa en poblaciones de Nothofagus antarctica (Forster) Oerst. del noroeste andino patagónico. Bosque 12, 53–59.
Premoli AC (1996) Allozyme polymorphisms, outerossing rates, and hybridization of South American Nothofagus. Genetica 97, 55–64.
| Allozyme polymorphisms, outerossing rates, and hybridization of South American Nothofagus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xit12lsr4%3D&md5=f73004a741000827606c1b6c2941ad85CAS |
Premoli AC, Steinke L (2008) Genetics of sprouting: effects of long‐term persistence in fire‐prone ecosystems. Molecular Ecology 17, 3827–3835.
| Genetics of sprouting: effects of long‐term persistence in fire‐prone ecosystems.Crossref | GoogleScholarGoogle Scholar | 18662228PubMed |
Press MC, Phoenix GK (2005) Impacts of parasitic plants on natural communities. New Phytologist 166, 737–751.
| Impacts of parasitic plants on natural communities.Crossref | GoogleScholarGoogle Scholar | 15869638PubMed |
Rawsthorne J, Watson DM, Roshier DA (2011) Implications of movement patterns of a dietary generalist for mistletoe seed dispersal. Austral Ecology 36, 650–655.
Reyes A, Muñoz M, Garcia H, Cox C (1986) Chemistry of Myzodendraceae, I. Myzodendrome, a new phenylbutanone of Myzodendron punctulatum. Journal of Natural Products 49, 318–320.
| Chemistry of Myzodendraceae, I. Myzodendrome, a new phenylbutanone of Myzodendron punctulatum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XksFOqsr4%3D&md5=166e104dd2208abef960d58ffa018a4fCAS |
Rolff J, Siva-Jothy MT (2003) Invertebrate ecological immunology. Science 301, 472–475.
| Invertebrate ecological immunology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXls1Cqsrc%3D&md5=45db439cb8dc454bdd38557ab9d211c8CAS | 12881560PubMed |
Schmid-Hempel P, Ebert D (2003) On the evolutionary ecology of specific immune defence. Trends in Ecology & Evolution 18, 27–32.
| On the evolutionary ecology of specific immune defence.Crossref | GoogleScholarGoogle Scholar |
Smith RB, Wass EF (1976) Field evaluation of ecological differentiation of dwarf mistletoe on shore pine and western hemlock. Canadian Journal of Forest Research 6, 225–228.
| Field evaluation of ecological differentiation of dwarf mistletoe on shore pine and western hemlock.Crossref | GoogleScholarGoogle Scholar |
Snyder MA, Fineschi B, Linhart YB, Smith RH (1996) Multivariate discrimination of host use by dwarf mistletoe Arceuthobium vaginatum subsp. cryptopodum: inter-and intraspecific comparisons. Journal of Chemical Ecology 22, 295–305.
| Multivariate discrimination of host use by dwarf mistletoe Arceuthobium vaginatum subsp. cryptopodum: inter-and intraspecific comparisons.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhvFSjsrs%3D&md5=b3a4d46fb86047a932e8ac2925e4e2c0CAS | 24227411PubMed |
Steinke LR, Premoli AC, Souto CP, Hedrén M (2008) Adaptive and neutral variation of the resprouter Nothofagus antarctica growing in distinct habitats in north-western Patagonia. Silva Fennica 42, 177
| Adaptive and neutral variation of the resprouter Nothofagus antarctica growing in distinct habitats in north-western Patagonia.Crossref | GoogleScholarGoogle Scholar |
Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends in Ecology & Evolution 14, 179–185.
| The ecology and evolution of plant tolerance to herbivory.Crossref | GoogleScholarGoogle Scholar |
Swofford DL, Selander RB, Black WC (1997) ‘BIOSYS-2: a computer program for the analysis of allelic variation in genetics. Computer software and manual.’ (University of Illinois at Urbana-Champaign: Champaign, IL, USA)
Tercero-Bucardo N, Kitzberger T (2004) Características del establecimiento e historia de vida de Misodendrum punctulatum (Misodendraceae) un muérdago de Sudamérica austral. Revista Chilena de Historia Natural 77, 509–521.
Tercero-Bucardo N, Rovere AE (2010) Patrones de dispersión de semillas y colonización de Misodendrum punctulatum (Misodendraceae) en un matorral postfuego de Nothofagus antarctica (Nothofagaceae) del noroeste de la Patagonia. Revista Chilena de Historia Natural (Valparaiso, Chile) 83, 375–386.
| Patrones de dispersión de semillas y colonización de Misodendrum punctulatum (Misodendraceae) en un matorral postfuego de Nothofagus antarctica (Nothofagaceae) del noroeste de la Patagonia.Crossref | GoogleScholarGoogle Scholar |
Thomson VE, Mahall BE (1983) Host specificity by a mistletoe, Phoradendron villosum (Nutt.) Nutt. subsp. villosum, on three oak species in California. Botanical Gazette 144, 124–131.
| Host specificity by a mistletoe, Phoradendron villosum (Nutt.) Nutt. subsp. villosum, on three oak species in California.Crossref | GoogleScholarGoogle Scholar |
van Baalen M, Beekman M (2006) The costs and benefits of genetic heterogeneity in resistance against parasites in social insects. American Naturalist 167, 568–577.
| The costs and benefits of genetic heterogeneity in resistance against parasites in social insects.Crossref | GoogleScholarGoogle Scholar | 16670998PubMed |
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 |
Williams CN (1959) Resistance of Sorghum to witchweed. Nature 184, 1511–1512.
| Resistance of Sorghum to witchweed.Crossref | GoogleScholarGoogle Scholar |
Yoder JI, Scholes JD (2010) Host plant resistance to parasitic weeds; recent progress and bottlenecks. Current Opinion in Plant Biology 13, 478–484.
| Host plant resistance to parasitic weeds; recent progress and bottlenecks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpt1Ojs74%3D&md5=f035916b6cf8b635bdf4937e3de2bd1eCAS | 20627804PubMed |
