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John W. Taylor & Mary L. Berbee. 2006 Mycologia, 98(6), 2006, pp. 838–849. # 2006 by The Mycological Society of America, Lawrence, KS 66044-8897 Dating divergences in the Fungal Tree of Life: review and new analyses John W. Taylor1 continuous records of fossil fungi, or their spores, Department of Plant and Microbial Biology, 111 that show recognizable shifts in morphology. Koshland Hall, University of California, Berkeley, Key words: dating divergences, fossil fungi, California 94720-3102 molecular phylogeny Mary L. Berbee Department of Botany, University of British Columbia, INTRODUCTION AND REVIEW Vancouver, British Columbia, V6T 1Z4 Canada Evolutionischangeovertimeandtimeisthe common currency that lets evolutionary biologists Abstract: The collection of papers in this issue of compare historical events in their group with events Mycologia documents considerable improvements in in other groups. Dating evolutionary events began taxon sampling and phylogenetic resolution regard- with evaluation of the geologic record and fossils, but ing the Fungal Tree of Life. The new data will when genetic variation could be conveniently de- stimulate new attempts to date divergences and tected, initially by protein electrophoresis, it also was correlate events in fungal evolution with those of employed to date evolutionary events (Zuckerkandl other organisms. Here, we review the history of dating and Pauling 1965, Sarich and Wilson 1967). Access to fungal divergences by nucleic acid variation and then nucleic acid sequence made the genetic contribution use a dataset of 50 genes for 25 selected fungi, plants only stronger and now it is with a combination of and animals to investigate divergence times in paleontology and molecular evolution that biologists kingdom Fungi. In particular, we test the choice of attempt to date divergences in the Tree of Life from fossil calibration points on dating divergences in near the present to the period of the last common fungi. At the scale of our analysis, substitution rates ancestor of life. Estimates of dates for events that varied without showing significant within-lineage occurred as many or more than 1 000 000 000 y ago correlation, so we used the Langley-Fitch method in cannot be exact and it is not surprising that there are the R8S package of computer programs to estimate competing estimates that differ greatly in time. Here node ages. Different calibration points had a dramatic we review the history of dating fungal divergences and effect on estimated divergence dates. The estimate for possible reasons for discrepancies in the process in the age of the Ascomycota/Basidiomycota split was the hope that recent advances in methods of 1 808 000 000 y ago when calibrated assuming that estimating divergences from molecular data and mammals and birds diverged 300 000 000 y ago, critical evaluation of fossils might help resolve this 1 489 000 000 y ago when calibrated assuming that controversy. After this review we examine substitution the 400 000 000 y old fungal fossil Paleopyreno- rate heterogeneity and the effect of fossil calibration on dating fungal divergences with sequence for 50 mycites devonicus represents Sordariomycetes and genes sampled from available genome sequences of ,400 000 000 y ago when calibrated assuming animals, plants and a broad sampling of fungi. 206 000 000 y ago for the plant eudicot/monocot Mycologists were quick to use nucleic acid sequence divergence. An advantage of a date of ,400 000 000 y variation to date important events in the history of ago for the Ascomycota/Basidiomycota divergence is fungal evolution and to use those dates to compare that the radiation of fungi associated with land plants events in fungal evolution to those of plants and would not greatly precede the earliest land plant animals. Fungi are good subjects for such studies fossils. Acceptance of ,400 000 000 y ago for the because they are for the most part haploid, have Ascomycota /Basidiomycota split would require that relatively few multigene families and many taxa are P. devonicus be considered a deeply branching large enough, particularly compared to other mi- Ascomycota. To improve on current estimates of crobes, to leave useful fossils, most often associated divergence times, mycologists will require calibration with plants (Taylor et al 2005). The field was points from within groups of fungi that share similar inaugurated by Simon et al (1993), who asked if the substitution rates. The most useful calibration is likely radiation of arbuscular mycorrhizal fungi coincided to depend on the discovery and description of with the appearance of green plants on land. Their analysis of 12 Glomeromycota small subunit riboso- Accepted for publication 25 September 2006. mal DNA (SSU rDNA) sequences, using parsimony 1 Corresponding author. E-mail: [email protected] analysis and calibration points of 200 000 000 y ago 838 TAYLOR AND BERBEE:DATING FUNGAL DIVERGENCES 839 for the origin of monocots and 1 000 000 000 y ago study (Doolittle et al 1996). This calibration increased for the divergence of fungi and plants, dated the the gap between molecular and fossil estimates of radiation of Glomeromycota at 462 000 000– divergences. However, as noted by the authors, this 353 000 000 y ago. These dates were compared to analysis failed to adequately account for the afore- fossils of arbuscular mycorrhizae in the rhizomes of mentioned Paleopyrenomycites fossil as a sordariomy- plants in the Rhynie chert (Pirozynski and Dalpe cete from 400 000 000 y ago (Berbee and Taylor 1989, Remy et al 1994) to support the hypothesis that 2001). Heckman et al (2001) took the most innovative mycorrhizal mutualisms of plants and arbuscular step in molecular analysis in 2001 when they revisited mycorrhizal fungi conquered land together. the evolution of land plants and associated arbuscular Also in 1993, Berbee and Taylor fit a broad mycorrhizae by expanding the nucleic acid database phylogenetic analysis of fungi to the geologic time- to include multiple protein coding genes and scale. They also used SSU rDNA sequences and estimating divergence times either by averaging the analysis by parsimony and neighbor joining, the latter dates estimated by the different protein genes or by with maximum likelihood distances, to determine concatenating them before averaging. The topology a phylogeny for fungi. They sorted fungi into nine estimated by the proteins was not in conflict with that lineages and showed, via relative rate tests, that the estimated from SSU rDNA, but the divergence times lineages had different rates of nucleotide substitu- were much older, further increasing the gap between tion. A mean rate was calculated and the rates on each divergences estimated from nucleic acid variation and lineage were normalized to make a tree with one those estimated from fossils. For example the global rate of nucleotide substitution (1.0% per radiation of Glomeromycota (ca. 1 200 000 000 y 100 000 000, for SSU rDNA). This tree was fit to the ago) now would predate the appearance of arbuscular geologic timescale using fungal fossils, fossils of mycorrhizal fossils (400 000 000 y ago) by ca. organisms associated with fungi (beetle galleries) or 800 000 000 y; however the new molecular diver- radiations of organisms mutualistic with fungi (rumi- gence dates accommodated the 400 000 000 y old nates). From these calibrations, the divergence of Paleopyrenomycites fossil. The key reason that the fungi and animals was estimated to have occurred at divergence times of Heckman et al were much older is 600 000 000 y ago. that a previous study by the same research group, The publications of 1993 have been influential, using the same multiprotein approach and fossil judging from their citations (Simon et al [1993] at evidence for the divergence of mammals and birds, 224 and Berbee and Taylor [1993] at 200), and these estimated the divergence of animals and fungi at ca. numbers show that dating evolutionary events has 1 576 000 000 y ago (Wang et al 1999). become an integral part of fungal phylogenetic studies, nowhere more important than with symbioses Fossils define minimum ages of divergence.—Some of whether they involve mycorrhizae, insects or humans. the gap between molecular and fossil dates certainly In addition to the application of molecular analyses, can be attributed to the fact that fossils usually new fossil finds have been reported; especially provide only a minimum age for divergences. There noteworthy were two fossils, one identified as Glo- are several well understood reasons for this observa- meromycota from 460 000 000 y ago (Redecker et al tion, which have been explored in depth for plants 2000) and another identified as a perithecial ascomy- (Magallon 2004). Simply put, all divergences begin cete and classified as a pyrenomycete (Sordariomy- when an ancestral species splits to form progeny cetes) that was found in the stem and rhizomes of the species; as a result, until morphological differences fossil plant Asteroxylon mackie from 400 000 000 y ago characteristic of the descendent groups develop, (Taylor et al 1999), which later was described as fossils of the different clades will not be recognizable Paleopyrenomycites devonicus (Taylor et al 2005) as such. In addition neither fossilization nor fossil (FIG. 1). discovery favor preservation and recovery of the In terms of molecular analyses, it was not until 2001 earliest fossils for any lineage. The problem is that the field shifted direction as much as in 1993, by compounded when the organisms of interest are which time phylogenetic methods employing likeli- microbes, but the problems remain even for charis- hood had been developed that could enforce matic macrofauna. For example there is controversy a constant molecular clock. Berbee and Taylor even about the vertebrate fossils that document the (2001) revisited fitting the fungal SSU rDNA tree to divergence of birds and mammals, which provide the geologic time with maximum likelihood analysis and geologic calibration for the 1 576 000 000 y old calibrating dates on this tree using an earlier date for estimate of animal-fungal divergence (Wang et al the divergence of animals and fungi, 965 000 000 y 1999).
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