| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Systematics, Phytogeography, and Evolution |
Department of Botany, MRC 166, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560-0166 USA
Received for publication August 22, 2000. Accepted for publication February 9, 2001.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
|---|
Key Words: Cladonia • cospeciation • host switching • ITS rDNA • lichens • parallel cladogenesis • phylogeny • symbiosis
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
|---|
; however, see Ahmadjian, 1993
, p. 5), lichen symbionts are often hypothesized to have undergone long-term coevolution, especially when one or both symbionts appear obligate and specialized (Ahmadjian, 1987
). However, coevolution has not been rigorously tested for lichen associations. To demonstrate coevolution directly requires an assessment of increased fitness resulting from reciprocal genetic change (Thompson, 1994
), although coevolution could be demonstrated indirectly by showing parallel cladogenesis or cospeciation between symbiont lineages (Page and Hafner, 1996
). A hypothesis of parallel cladogenesis would be accepted with highly specific associations between algal and fungal partners, especially if there is strict vertical transfer of inhabiting algal partners throughout a fungal lineage. In contrast, this hypothesis would be rejected in the case of horizontal transfer of algal partners among fungal lineages. This phylogenetic process is here called algal switching (and is distinct from the "cyanobiont/phycobiont switches" by an individual lichen-forming fungus of Hawksworth, 1988
). When reciprocal evolution leads to cospeciation, coordinated speciation events, equal numbers of species among symbiont partners should evolve—a situation not predicted from morphological studies of these algae (Tschermak-Woess, 1988
) and their fungal partners (Hawksworth et al., 1995
).
Cospeciation has been predicted for many symbiotic associations: lice with birds (Page et al., 1998
; see also, Clayton, Price, and Page, 1996
) or pocket gophers (Demastes and Hafner, 1993
; Hafner and Page, 1994
) and wasps in figs (Herre et al., 1996
); chemoautotrophic bacteria in bivalves (Distell, Felbeck, and Cavanaugh, 1994
; Peek et al., 1998
), bacteria in aphids (Clark et al., 2000)
and rhizobia in root nodules (Jeong, Ritchie, and Myrold, 1999
); arenaviruses in rodents (Bowen, Peters, and Nichol, 1997
); and fungi in plants (Schardl et al., 1997
) or with attine ants (Chapela et al., 1994
; Hinkle et al., 1994
; Mueller, Rehner, and Schultz, 1998
) and bark beetles (Six and Paine, 1999
). However, cospeciation is often obscured by host switching, resource tracking (Kethley and Johnston, 1975
), geographically patchy evolution (Thompson, 1999
), taxon sampling (Page, 1993
), and invalid assumptions in evolutionary models (Clark et al., 2000)
. More recently, host switching has been proposed in a number of symbiotic associations, even those where cospeciation was previously reported or partial cospeciation confirmed, as with endosymbiotic bacteria and aphids (Clark et al., 2000)
or clams (Peek et al., 1998
), respectively.
Among lichen associations, stealing of algal genotypes is known to occur in some lichen-forming fungi that are transiently parasitic on other lichen associations. For example, parasitic Diploschistes muscorum (Friedl, 1987
) first associates with the algal partner Trebouxia irregularis of its lichen host Cladonia and later its preferred partner Trebouxia showmanii. A recent study of overall algal partners in lichen communities has shown that algal morphospecies and genotypes are shared and, therefore, presumably switched among different species, genera, and families of lichen-forming fungi (Beck, Friedl, and Rambold, 1998
; see also, Ahmadjian, 1987
, and Rambold, Friedl, and Beck, 1998
). However, algal switching and cospeciation among lichen symbionts have not been tested with comparative phylogenetic methods and depend, at least in part, on traditional taxonomic concepts. We present rigorous phylogenetic tests of both relationships within and among species of each of the lichen partners and of the hypotheses of parallel cladogenesis and cospeciation between them. In the present study our goals were: (1) to examine algae in natural lichen associations with worldwide representatives of the diverse fungal family Cladoniaceae for cospeciation, parallel cladogenesis, and algal switching and (2) to identify sets of taxa for further study of lichen coevolution.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
|---|
|
and Ivanova et al. (1999)
. DNA, suspended in dH2O, was amplified by the polymerase chain reaction (PCR). Initial amplification of the ITS1, ITS2, and 5.8S regions was from universal primers annealing in the nuclear small subunit (SSU) ribosomal DNA (rDNA), nu-SSU-1583-5' (CAACGAGGAATTCCTAGT; SR18R in DePriest, 1993
) and in the nuclear large subunit (LSU) rDNA, ITS4–3' (TCCTC CGCTTATTGATATGC; White et al., 1990
). Subsequent amplifications were from newly designed primers that discriminated between algal and fungal sequences. Algal specific primer nr-SSU-1780-5'Algal spanned the 3'SSU rDNA and ITS1 junction, (5'-CTGCGGAAGGATCATTGATTC-3') and nr-LSU-0012-3' Algal, a variable region of the LSU rDNA, (5'-AGTTCAGCGGGTGGTCTTG-3'). Fungal specific primers were at the same locations, nr-SSU-1780-5' Fungal (5'-CTGCGGAAGGATCATTAATGAG-3'), and nr-LSU-0012-3' Fungal (5'-AGTTCAGCGGGTATCCCT-3'), respectively. Amplifications were performed in 100 µL reactions (10 mmol/L Tris-HCl pH 8.8, 1.5 mmol/L MgCl2, 50 mmol/L KCl, 0.1% Triton X-100), with 1.25 units Klentaq 1 (AB Peptides, St. Louis, Missouri, USA), 200 µmol/L of each dNTP, 0.5 µmol/L of primers, and between 1.0 and 10 ng of DNA. Amplification conditions in Perkin Elmer (Foster City, California, USA) Cetus 480 or 9700 thermal cyclers were: template denaturing at 94°C for 60 s, primer annealing at 50°C for 60 s, and primer extension at 72°C for 2 min (extended by 5 s per cycle) for 30 cycles. PCR products were cleaned with Wizard PCR Preps (Promega, Madison, Wisconsin, USA) and quantified on 1% agarose gel stained with ethidium bromide.
DNA sequencing and sequence alignment
Double-stranded products were sequenced using the PRISM Ready Reaction DyeDeoxy Terminator Cycle Sequencing Kit (Applied Bio-Systems, Foster City, California, USA), following the manufacturer's instructions, in a Perkin Elmer Cetus 9700 thermal cycler with detection on a 373 Automatic Sequencer (Applied Bio-Systems) from primers described above as well as ITS3–5' and ITS2–3' (White et al., 1990
). Excess dyedeoxy terminators were removed by filtration through Sephadex G-50 Fine (Pharmacia). Sequences were assembled into full-length sequences using Sequence Navigator 1.0 (Applied Bio-Systems); both strands were sequenced from multiple primers. Sequences representing the SSU rDNA, SSU rDNA insertions or introns, and LSU were removed and only the ITS sequences used for the analysis. ITS sequences from 73 algal partners or Trebouxia cultures and from 33 fungal partners were aligned manually in PAUP 4.0d65 (Swofford, 1998
).
Phylogenetic analyses
Aligned sequences from each of the algal and fungal data sets were subjected to two methods of phylogenetic analysis, maximum likelihood and maximum parsimony, using PAUP 4.0d65. All nucleotide positions of ITS1 and ITS2 were included in the analyses and alignment gaps were treated as missing data; nucleotide positions representing the 5.8S were excluded from the analyses. Maximum parsimony was performed using the options tree bisection and reconnection (TBR) branch swapping, collapse zero length branches, and acctran character-state optimization. Heuristic searches were conducted using 100 random addition replicates with a limit of 1000 trees per search and bootstrap searches of 500 resamplings (Felsenstein, 1985
). All trees were unrooted. Maximum likelihood analysis used HKY85 model (Hasagawa, Kishino, and Yano, 1985
) with two substitution types and an estimated ti/tv (transition/transversion) ratio. Maximum likelihood (ML) trees were found by random addition of taxa in 100 replications. The fungal trees were obtained using the same search parameters except there was no limit applied to the number of trees saved per search. Because it is more likely that two trees will be congruent if one or both contain little phylogenetic signal, the skew (g1) in the distributions of tree length was measured using the "evaluate random trees" option in PAUP 4.0 and compared with critical values in Hillis and Huelsenbeck (1992)
.
Incongruence tests were performed for tree topologies and subsets of the data. Tree topologies were compared using the Kashino-Hasagawa and Templeton tests performed in PAUP (phylogenetic analysis using parsimony) using parsimony treescore options (Kashino-Hasagawa and nonparametric tests, respectively), and Rodrigo's second test (Rodrigo et al., 1993
) using the filter tree option. The partition homogeneity test was also implemented in PAUP and was used for the Incongruence Length Difference (ILD) test. Cospeciation events in algal and fungal phylogenies were estimated using TreeMap 1.0 (Page, 1995
). The algal topology was mapped onto the fungal topology using an exact search to find all the best reconstructions. The algal and fungal topologies were taken from the fully resolved maximum likelihood trees. The topologies each contained 22 taxa because some of the algal taxa that were identical had to be excluded to produce fully dichotomized topologies. To test whether reconstructed cospeciation events could be due to chance alone, 1000 random parasite (algal) trees were generated using the Markovian model (Harding, 1971
) and the maximum number of cospeciation events was estimated between each pair of random host (fungal) and parasite (algal) trees. A P > 0.05 does not reject the null hypothesis that the cospeciation events were due to chance alone.
|
RESULTS AND DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
|---|
recently proposed that Cladoniaceae symbionts may represent the genus Asterochloris sensu Friedl.
Algal sequences from the 57 natural lichen associations were highly similar, even though they were from dispersed geographic locations and with different representatives of Cladoniaceae. Pairwise ITS sequence similarities among algal symbionts of the natural lichen associations were >95%. Pairwise ITS sequence similarities among the symbionts from natural lichen associations and 11 of the cultures were >93%; similarity among the 11 putative "Asterochloris" cultures was >97%. They were almost identical to the ITS sequence reported earlier for lichen symbiont Trebouxia erici (DePriest, 1992
). However, ITS sequences from three remaining cultures (T. impressa, UTEX culture 893 GenBank accession # AF345890, UTEX culture 892 accession # AF345891; and T. asymmetrica, UTEX culture 2507 accession # AF345889) and some other available sequences from lichen-forming algae (T. impressa, accession number AJ007388; T. jamesii, Z68700 and Z68699; and T. arboricola Z68703) could not be aligned to the "Asterochloris" sequences. Therefore, the "Asterochloris" algal symbionts are apparently distinct from those of Trebouxia sensu stricto as proposed by Rambold, Friedl, and Beck (1998)
.
When sequences were compared among paired algal and fungal partners from 33 Cladoniaceae associations, there were 24 distinct algal genotypes, and similarities among genotypes were very high, 95–100%. Similarities among fungal genotypes were by comparison relatively low, 81–98%. Therefore, there is substantially less variation among the algal symbionts relative to that of their fungal partners. This difference could indicate a longer time of divergence or higher mutation rate in the fungi, strong fungal selection of algal genotypes, or population processes leading to genotypic fixation in the algae (Nuismer, Thompson, and Gomulkiewicz, 1999
). Because random amplified polymorphic DNA (RAPD) analysis with 23 primers showed little polymorphism among "Asterochloris" cultures of algae with similar ITS sequences (data not shown), the lack of ITS variation in this study may reflect a low level of variation across the entire algal genome.
Maximum likelihood analysis of the 70 aligned sequences found a single most likely topology (Fig. 1), identical to one of the trees found in maximum parsimony (MP) analysis. Both the unrooted ML network and the MP consensus showed two clades separated by sequences from cultured Trebouxia erici and the algal symbiont of Stereocaulon dactylophyllum. One of the clades, Clade I (bootstrap support 100%) encompassed "Asterochloris" morphospecies Trebouxia glomerata, T. irregularis, and T. pyriformis, along with 33 natural lichen-forming algae. The lack of resolution within Clade I, the near identity of these ITS sequences (>98.5%), and the similarity of T. glomerata and T. pyriformis RAPD amplification patterns support the assertion that they may represent genotypes of a single species, T. irregularis, as previously reported by Friedl (1989)
. Preliminary data predict comparable sequence homogeneity among their mitochondrial large and small subunit rDNA (>99%). The Clade I genotypes associate with fungi of different genera, families, and even orders because four cultures were isolated from associations with Stereocaulon (Stereocaulaceae, Lecanorales) and two algal sequences were amplified from Pycnothelia papillaria (Cladoniaceae, Lecanorales) and Anzina carnionivea (Trapeliaceae, possibly Agyriales). This is in agreement with Hildreth and Ahmadjian's (1981)
earlier report that a single species, or in this case even genotype, of alga may form associations with taxonomically unrelated lichens, even those differing in growth form (fruiticose Cladonia vs. crustose Anzina) and geographic location (Table 1).
|
showed that there are no MP topologies in common between the two data sets, indicating that fungal topologies were not estimates of the algal phylogeny. The Kashino-Hasagawa (Kashino and Hasagawa, 1989
) and Templeton's tests (Templeton, 1983
) produced P values <0.05, indicating that topologies from the two data sets were significantly different. Since the P value for the partition homogeneity test (incongruence length difference, ILD; Farris et al., 1994
) was <0.05, the characters in the algal and fungal data sets were incongruent. However, Clark et al. (2000)
suggested that these tests may be confounded by different rates of evolution between symbiotic partners or even gene regions, as shown in our rejection of the combinability of even the linked ITS1 and 2 regions (Table 3). Using a randomization test implemented in TreeMap, the null hypothesis that "the parasite [algal] phylogeny is independent of the host [fungal] phylogeny" (Page, 1994
) was not rejected since the P value was >0.05, which excluded the possibility of comparing rates of symbiont evolution (Huelsenbeck, Rannala, and Yang, 1997
). The rejection of parallel cladogenesis in these five tests suggests that vertical transmission alone cannot account for the current symbiont associations. Therefore, horizontal transfer or algal switching must be ongoing even within the Cladoniaceae.
|
|
|
The ongoing debate in lichenology over whether the lichen-forming algae live independently or are obligately associated with their fungal partners (citations in Honegger, 1998
, and Ahmadjian, 1988, 1993
, respectively) is not resolved by this evidence for algal switching. As noted by Honegger (1998)
, both the algal and fungal partners can be cultured axenically and, therefore, are not physiologically dependent on the symbiotic association, although they may be ecologically dependent. The 3–5 algal switching events required for our reconstructions are consistent with lichen-forming algae living independent of their fungal symbiont and with different fungal species selecting the same genotype from a "pool of locally available algae" (Beck, Friedl, and Rambold, 1998
). Most Cladoniaceae fungi reproduce sexually, and their spores, discharged from the nurturing symbiosis, in theory must quickly recruit new algal partners from a local "pool." However, even if algae are obligated to lichen associations, then algal switching could occur when fungi steal their algae from other intact associations. Friedl (1987)
proposed that in some cases a secondary fungus such as Diploschistes muscorum may invade a lichen thallus and take its algal symbiont; such inter-Cladonian associations have been reported in a few situations (see Rambold and Triebel, 1992
, p. 106). Robinson (1975)
and Ott (1987)
proposed that some of these fungi take algae from soredia, special packets of algae and fungi that are easily dispersed. Long-distance dispersal of Cladoniaceae soredia would present these algal genotypes for switching to other lichens. Our analysis cannot distinguish among methods of horizontal transfer that may occur among lichen associations (Friedl, 1987
).
We provide statistical evidence to reject overall cospeciation and to support horizontal switching of algal genotypes among their fungal symbionts. Although parallel cladogenesis could not be supported across these paired data sets, cospeciation events may yet be detected in isolated clades of Cladonia fungi (Fig. 2). Some of the 10–11 putative cospeciation events mapped onto the algal phylogeny were common among different reconstructions. These cospeciation events were located within the clade containing C. peltastica, C. spinea and C. pulviniformis, all collected from the Guiana Shield of South America, as well as the clade containing C. furcata, C. farinacea, and C. turgida (Fig. 2). However, this result may be confounded by the geographic distribution of some algal genotypes.
Intimate symbioses such as lichen associations are hypothesized to promote loss of sexual reproduction and lower speciation rates of symbionts enclosed by their partners (as mutualisms; Law and Lewis, 1983
). This is in agreement with some observations that sexual reproduction by Trebouxia is suppressed in lichen associations (Friedl and Büdel, 1996
). However, others have reported algal zoospore production that, when released from a thallus, could form sexually reproducing free-living microcolonies of Trebouxia. Sexual products of these microcolonies could then reenter into lichen associations (Slocum, Ahmadjian, and Hildreth, 1980
). In our observations, 46 fungal species from five continents are associated with only 36 genotypes, representing perhaps four or fewer species of algae. Although lack of algal specificity could be explained by relatively recent algal switches (horizontal transfer), this would require efficient and recent dispersal of algal genotypes over continental distances independent of that of their fungal partners. Perhaps long-distance dispersal of the algae and accompanying high selectivity by the fungus (Tschermak-Woess, 1988
; Beck, Friedl, and Rambold, 1998
), can provide an explanation for the broad geographic homogeneity of algal ITS genotypes.
This study demonstrates that there are very few algal genotypes shared among variously related taxa of the family Cladoniaceae, implying that selectivity is not equal between lichen-forming fungi and algae. The fungi may be selecting very specific algal genotypes, while the algae are tolerant of many fungal partners. If fungi can select free-living algae, or even those from other lichen associations, then this horizontal transfer (algal switching) can explain the symbiotic association of algae and fungi with incongruent phylogenetic histories. This would support the common model of the lichen symbiosis as a "domestication" of photosynthetic algae by the heterotrophic fungi (see Ahmadjain, 1993
), analogous to human agriculture in the selection and distribution of crops across cultural lineages or the evolution of agriculture in ants (Mueller, Rehner, and Schultz, 1998
). We propose that horizontal transfer of algae, long-distance dispersal, and high selectivity by the fungus of algal genotypes allow a superior genotype to sweep through populations of taxonomically and geographically diverse lichens. This would support Law's (1985)
hypothesis that through natural selection genotypes of symbionts are produced that are so accommodating they could be transferred even among unrelated hosts.
|
|
FOOTNOTES |
|---|
2 Author for reprint requests, current address: 525 Buller Building, Department of Botany, University of Manitoba, Winnipeg, Manitoba R3T 2N2 Canada.
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
|---|
———. 1988 The lichen alga Trebouxia: does it occur free-living?. Plant Systematics and Evolution 158: 243-247[CrossRef][ISI]
———. 1993 The lichen symbiosis. John Wiley and Sons, New York, New York, USA
Beck A. T. Friedl G. Rambold 1998 Selectivity of photobiont choice in a defined lichen community: inferences from cultural and molecular studies. New Phytologist 139: 709-720[CrossRef][ISI]
Bowen M. D. C. J. Peters S. T. Nichol 1997 Phylogenetic analysis of the Arenaviridae: patterns of virus evolution and evidence for cospeciation between areanaviruses and their rodent hosts. Molecular Phylogenetics and Evolution 8: 301-316[CrossRef][ISI][Medline]
Chapela I. H. S. A. Rehner T. R. Schultz U. G. Mueller 1994 Evolutionary history of the symbiosis between fungus-growing ants and their fungi. Science 266: 1691-1694
Clark M. A. N. A. Moren P. Bauman J. J. Wernegreen 2000 Cospeciation between bacterial endosymbionts (Buchnera) and recent radiation of aphids (Uroleucon) and pitfalls of testing for phylogenetic congruence. Evolution 54: 517-525[CrossRef][ISI][Medline]
Clayton D. H. R. D. Price R. D. M. Page 1996 Revision of Dennyus (Collodennyus) lice (Phthiraptera: Menoponidae) from swiftlets, with descriptions of new taxa and a comparison of host–parasite relationships. Systematic Entomology 21: 179-204[CrossRef][ISI]
Demastes J. W. M. S. Hafner 1993 Cospeciation of pocket gophers (Geomys) and their chewing lice (Geomydoecus). Journal of Mammalogy 74: 521-530[CrossRef]
DePriest P. T. 1992 Molecular-genetic analysis of ribosomal DNA polymorphism in the Cladonia chlorophaea complex. Duke University, Durham, North Carolina, USA and University Microfilms International, Michigan, USA
———. 1993 Small subunit rDNA variation in a population of lichen fungi due to optional group-I introns. Gene 134: 67-74[CrossRef][ISI][Medline]
Distell D. L. H. Felbeck C. M. Cavanaugh 1994 Evidence for phylogenetic congruence among sulfur-oxidizing chemoautotropic bacterial endosymbionts and their bivalve hosts. Journal of Molecular Evolution 38: 533-542[CrossRef][ISI]
Farris J. S. M. Kallersjo A. G. Kluge C. Bult 1994 Permutations. Cladistics 10: 65-76[CrossRef][ISI]
Felsenstein J. 1985 Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-791[CrossRef][ISI]
Friedl T. 1987 Thallus development and phycobionts of the parasitic lichen Diploschistes muscorum. Lichenologist 19: 183-191
———. 1989 Systematik und Biologie von Trebouxia (Microthamniales, Chlorophyta) als Phycobiont der Parmeliaceae (lichenisierte Ascomyceten). Universität Bayreuth
———, and B. Büdel 1996 Photobionts. In T. H. Nash III [ed.], Lichen biology, 8–23. Cambridge University Press, Cambridge, UK
Grube M. P. T. DePriest A. Gargas J. Hafellner 1995 DNA isolation from lichen ascomata. Mycological Research 99: 1321-1324[ISI]
Hafner M. S. R. D. M. Page 1994 Molecular phylogenies and host-parasite cospeciation: gophers and lice as a model system. Philosophical Transactions of the Royal Society of London, B, Biological Sciences 349: 77-83
Harding E. F. 1971 The probabilities of rooted tree-shapes generated by random bifurcation. Advances in Applied Probability 3: 44-77
Hasagawa M. H. Kishino T. Yano 1985 Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22: 160-174[CrossRef][ISI][Medline]
Hawksworth D. L. 1988 Coevolution of fungi with algae and cyanobacteria in lichen symbioses. In K. A. Pirozynski and D. L. Hawksworth [eds.], Coevolution of fungi with plants and animals, 125–148. Academic Press, London, UK
———,P. M. Kirk B. C. Sutton D. N. Pegler 1995 Dictionary of the fungi, 8th ed. International Mycological Institute, Cambridge University Press, Cambridge, UK
Herre E. A. C. A. Machado E. Bermingham J. D. Nason D. M. Windsor S. S. McCafferty W. Van Houten K. Bachmann 1996 Molecular phylogenies of figs and their pollinator wasps. Journal of Biogeography 23: 521-530[CrossRef][ISI]
Hildreth K. C. V. Ahmadjian 1981 A study of Trebouxia and Pseudotrebouxia isolates from different lichens. Lichenologist 13: 65-86
Hillis D. M. J. P. Huelsenbeck 1992 Signal, noise, and reliability in molecular phylogenetic analyses. Journal of Heredity 83: 189-195
Hinkle G. J. K. Wetter T. R. Schultz M. L. Sogin 1994 Phylogeny or the attine ant fungi based on analysis of small subunit ribosomal RNA gene sequences. Science 266: 1695-1697
Honegger R. 1998 The lichen symbiosis—what is so spectacular about it?. Lichenologist 30: 193-212[ISI]
Huelsenbeck J. P. B. Rannala Z. Yang 1997 Statistical tests of host–parasite cospeciation. Evolution 51: 410-419[CrossRef][ISI]
Ivanova N. V. P. T. Depriest V. K. Bobrova A. V. Troitsky 1999 Phylogenetic analysis of the lichen family Umbilicariaceae on the basis of nuclear SSU, ITS1, 5.8S and ITS2 rDNA sequences. Lichenologist 31: 477-489[ISI]
Jeong S. C. N. J. Ritchie D. D. Myrold 1999 Molecular phylogenies of plants and Frankia support multiple origins of actinorhizal symbioses. Molecular Phylogenetics and Evolution 13: 493-503[CrossRef][ISI][Medline]
Kashino H. M. Hasagawa 1989 Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. Journal of Molecular Evolution 29: 170-179[CrossRef][ISI][Medline]
Kethley J. B. D. E. Johnston 1975 Resource tracking patterns in bird and mammal ectoparasites. Miscellaneous Publications of the Entomological Society of America 9: 231-236
Law R. 1985 Evolution in a mutualistic environment. In D. H. Boucher [ed.], The biology of mutualism: ecology and evolution, 145–170. Oxford University Press, New York, New York, USA
———, and D. H. Lewis 1983 Biotic environments and the maintenance of sex—some evidence from mutualistic symbioses. Biological Journal of the Linnean Society 20: 249-276[CrossRef]
Mueller U. G. S. A. Rehner T. R. Schultz 1998 The evolution of agriculture in ants. Science 281: 2034-2038
Nuismer S. L. J. N. Thompson R. Gomulkiewicz 1999 Gene flow and geographically structured coevolution. Proceedings of the Royal Society London Series B 266: 605-609[CrossRef]
Ott S. 1987 Sexual reproduction and developmental adaptations in Xanthoria parietina. Nordic Journal of Botany 7: 219-228[ISI]
Page R. D. M. 1993 Genes, organisms and areas: the problem of multiple lineages. Systematic Biology 42: 77-84[CrossRef][ISI]
———. 1994 Parallel phylogenies: reconstructing the history of host–parasite assemblages. Cladistics 10: 155-173[CrossRef][ISI]
———. 1995 TreeMap 1.0. Division of Environmental and Evolutionary Biology, Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow, UK
———, and M. S. Hafner 1996 Molecular phylogenies and host–parasite cospeciation: gophers and lice as a model system. In P. H. Harvey, A. J. Leigh Brown, J. Maynard Smith, and S. Nee [eds.], New uses for new phylogenies, 255–272. Oxford University Press, New York, New York, USA
———,P. L. M. Lee S. A Becher R. Griffiths D. H. Clayton 1998 A different tempo of mitochondrial DNA evolution in birds and their parasitic lice. Molecular Phylogenetics and Evolution 9: 276-293[CrossRef][ISI][Medline]
Peek A. S. R. A. Feldman R. A. Lutz R. C. Vrijenhoek 1998 Cospeciation of chemoautotrophic bacteria and deep sea clams. Proceedings of the National Academy of Sciences, USA 95: 9962-9966
Rambold G. T. Friedl A. Beck 1998 Photobionts in lichens: possible indicators of phylogenetic relationships?. Bryologist 101: 392-397[ISI]
———, and D. Triebel 1992 The inter-Lecanoralean associations—Bibliotheca Lichenologica, 48. J. Cramer, Berlin, Germany
Robinson H. 1975 Considerations on the evolution of lichens. Phytologia 32: 407-413
Rodrigo A. G. K. Kelly-Borges P. R. Bergquist P. L. Bergquist 1993 A randomization test of the null hypothesis that two cladograms are sample estimates of a phylogenetic tree. New Zealand Journal of Botany 31: 257-268[ISI]
Schardl C. L. A. Leuchtmann K. R. Chung D. Penny M. R. Siegel 1997 Coevolution by common descent of fungal symbionts (Epichloe spp.) and grass hosts. Molecular Biology and Evolution 14: 133-143[ISI]
Six D. L. T. D. Paine 1999 Phylogenetic comparison of ascomycete mycangial fungi and Dendroctonus bark beetles. Annals of the Entomological Society of America 92: 159-166
Slocum R. D. V. Ahmadjian K. C. Hildreth 1980 Zoosporogenesis in Trebouxia gelatinosa: ultrastructure potential for zoospore release and implications for the lichen association. Lichenologist 12: 173-187[CrossRef][ISI]
Swofford D. 1998 Phylogenetic analysis using parsimony (PAUP) version 4.0. Sinauer, Sunderland, Massachusetts, USA
Templeton A. R. 1983 Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the humans and the apes. Evolution 37: 221-244[CrossRef][ISI]
Thompson J. N. 1994 The coevolutionary process. University of Chicago Press, Chicago, Illinois, USA
———. 1999 Specific hypotheses on the geographic mosaic of coevolution. American Naturalist 153: S1-S14[CrossRef][ISI]
Tschermak-Woess E. 1988 The algal partner. In M. Galun [ed.], CRC handbook of lichenology, vol. I, 39–92. CRC Press, Boca Raton, Florida, USA
White T. J. T. D. Bruns S. B. Lee J. W. Taylor 1990 Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, and T. J. White [eds.], PCR protocols: a guide to methods and applications, 315–322. Academic Press, New York, New York, USA
This article has been cited by other articles:
|
|
 |
|
  T. C. LaJeunesse "Species" Radiations of Symbiotic Dinoflagellates in the Atlantic and Indo-Pacific Since the Miocene-Pliocene Transition Mol. Biol. Evol., March 1, 2005; 22(3): 570 - 581. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
