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Flammable biomes dominated by eucalypts originated at the Cretaceous–Palaeogene boundary

Flammable biomes dominated by eucalypts originated at the Cretaceous–Palaeogene boundary ARTICLE DOI: 10.1038/ncomms1191 Received 20 may 2010 | Accepted 12 Jan 2011 | Published 15 Feb 2011 Flammable biomes dominated by eucalypts originated at the Cretaceous–Palaeogene boundary 1 2 3 1 4 michael D. Crisp , Geoffrey E. Burrows , Lyn G. Cook , Andrew H. Thornhill & David m. J. s. Bowman Fire is a major modifier of communities, but the evolutionary origins of its prevalent role in shaping current biomes are uncertain. Australia is among the most fire-prone continents, with most of the landmass occupied by the fire-dependent sclerophyll and savanna biomes. In contrast to biomes with similar climates in other continents, Australia has a tree flora dominated by a single genus, Eucalyptus, and related myrtaceae. A unique mechanism in myrtaceae for enduring and recovering from fire damage likely resulted in this dominance. Here, we find a conserved phylogenetic relationship between post-fire resprouting (epicormic) anatomy and biome evolution, dating from 60 to 62 ma, in the earliest Palaeogene. Thus, fire-dependent communities likely existed 50 million years earlier than previously thought. We predict that epicormic resprouting could make eucalypt forests and woodlands an excellent long-term carbon bank for reducing atmospheric Co compared with biomes with similar fire regimes in other continents. Division of Evolution, Ecology and Genetics, Research School of Biology, The Australian National University, Canberra, Australian Capital Territory 0200, 2 3 Australia. Institute for Land, Water and Society, Charles Sturt University, Locked Bag 588, Wagga Wagga, New South Wales 2678, Australia. School of Biological Sciences, The University of Queensland, Brisbane, Queensland 4072, Australia. School of Plant Science, Private Bag, Hobart, Tasmania 7001, Australia. Correspondence and requests for materials should be addressed to M.D.C. (email: mike.crisp@anu.edu.au). nATuRE CommunICATIons | 2:193 | DoI: 10.1038/ncomms1191 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. ARTICLE nATuRE CommunICATIons | DoI: 10.1038/ncomms1191 pen-canopied communities are far more extensive across persistence traits has been found in taxa occurring in fire-dependent the world than predicted by consideration of climate and communities. Biome adaptations in the Myrtaceae are significantly Osoil fertility alone . Moreover, boundaries between open conserved (tip randomization test, P < 0.001) and the transitions woodlands and closed-canopy rainforest are oen ft surprisingly that have occurred are strongly directional—all sclerophyll lineages 1,2 sharp . Fire is known to have a major role in maintaining open originated from a rainforest ancestor and all monsoonal savanna communities: both plot experiments and modelling show that, in the lineages arose more recently, from sclerophyll or rainforest ances- 2,3 absence of fire, closed forests would cover much of both Australia tors. Two-thirds (21) of biome shifts were into savanna, confirming 1 1 and the world —hence their definition as ‘fire-dependent’ . In that this biome is a sink relative to the other biomes and suggest- Australia this effect is extreme, with rainforest marginalized by fire ing that the advent of monsoonal climate opened a major ecologi- to a tiny portion (2%) of the continent and absent from much of cal opportunity that pre-adapted Myrtaceae were able to exploit the climatically and edaphically suitable landscape . Even the vast effectively. However, we found no support for the hypothesis that 4,5 central Australian arid zone is dominated by fire at frequencies this new environment (with its more frequent but less intense 6,18 similar to those in temperate grassy woodlands and dry sclerophyll fires ) exerted sufficient selection to alter the epicormic anatomy 6 1 forests (global modelling suggesting that this region is ‘bare’ is of the Myrtaceae overall (Pagel94 ML test, P = 0.137; Bayesian simplistic). In contrast with other continents, a single diverse family, stochastic mapping test, P = 0.2), except in Xanthostemon and Myrtaceae, dominates Australian fire-dependent woodlands and perhaps Melaleuca (Supplementary Fig. S1). By contrast, v fi e of the forests, with 1,600 species, including 800 eucalypts and their close seven transitions in epicormic resprouting anatomy coincided with relatives . Many are excellent post-fire epicormic resprouters from shifts between the everwet and sclerophyll biomes ( Table 1). 8–11 the stems and branches aer ft high-intensity fires . In most investi- gated angiosperm trees, dormant epicormic buds are situated in the Alternative reconstructions. e Th sequence of events at the base of 8,12 outer bark , where they are likely killed by fire, but in eucalypts, the eucalypts is unclear because of uncertain trait reconstructions at the epicormic bud-forming structures are located deeply, where nodes M and K (Figs 1 and 2; Supplementary Figs S1 and S2) and they are protected by the full thickness of the bark and can sprout lack of support for the position of Syncarpia. e Th inferred trait tran - even aer ft high-intensity fires . Moreover, the epicormic structures sitions shown in Table 1 are a shift into the sclerophyll biome with a of eucalypts appear unique, consisting not of buds but of narrow, gain of resprouting epicormic type A between nodes Y and K, and a radially oriented strips of cells of meristematic appearance, and as reversal of both traits in the Stockwellia clade (node Q). e Th alterna - 8–11 such differ from those recorded in other families . tive reconstruction infers an independent transition to sclerophyll Given the above, it has been hypothesized that evolution of fire and epicormic resprouting in each of Syncarpia and Eucalypteae, tolerance in Myrtaceae was directly linked with the origins and with retention of the ancestral everwet biome and epicormic res- expansion of the fire-dependent biomes in Australia, especially the prouting in the Stockwellia clade. e Th timing of these alternative 2,6,13 southern sclerophyll and northern savanna biomes . However, the reconstructions (62–55 Ma) is about the same as in the reconstruc- influence of wildfire on the evolution of Australian biomes through tions shown in the Figures and Table 1. e Th lack of branch length the Palaeogene, when Australia was still part of East Gondwana, has data for interpolated species within Syncarpia, Tristaniopsis and been little studied. e Th Australian fossil record has provided little Xanthostemon resulted in wide bounds on the timing estimates direct evidence of fire (fusain charcoal) before the mid-Miocene, of transitions within these lineages (Table 1). Reversals to non- when the climate aridified and charcoal levels increased dramati - resprouting types occurred within Melaleuca, whose most recent 2,14 cally . Here, we show that specialized epicormic resprouting origi- common ancestor reconstructs as a resprouter occurring in the nated in the eucalypt lineage much earlier, at least 60 million years sclerophyll biome. e Th timing of these shifts is uncertain because of ago. We find a significant link between the evolution of this unique lack of branch length information within the group. anatomy and the timing of shifts by Myrtaceae into the flammable sclerophyll biome. However, there was no statistical association with Discussion the more recent shifts into the monsoonal biome, which experiences We have shown that both epicormic resprouting in Myrtaceae more frequent but less intense fires. Our results contrast with the and flammable sclerophyll biomes likely originated in the earliest current view that fire-dominated vegetation originated much later, Cenozoic, 60–62 Ma, and that their evolution is significantly linked. aer ft global climate aridified and the monsoonal biome developed, In eucalypts, the distinctive epicormic resprouting anatomy has 14–16 in the late Miocene . been strictly conserved until the present, despite changes in habitat and response to fire. For example, Eucalyptus brachyandra grows on Results fire-protected cliffs and E. regnans dominates wet sclerophyll for- Ancestral biomes and epicormic structures. Using trait mapping est and, although usually killed by high-intensity fires, still retains on a dated molecular phylogeny, we found that both epicormic capacity to resprout epicormically aer les ft s intense fires . resprouting in Myrtaceae and their adaptation to the sclerophyll Sclerophyllous morphology is oen ft assumed to be an adapta - 13,19,20 biome probably evolved in the earliest Palaeogene, 60–62 Ma (Figs 1 tion to fire and a driver of diversification , but sclerophylly has and 2; Table 1; Supplementary Figs S1 and S2). e Th myrtoid ancestor diverse functions and is not necessarily an indicator of climates in 2,21,22 reconstructs as a non-resprouting inhabitant of rainforest (Table 1; general or fire-prone vegetation in particular . Nevertheless, in Fig. 1; Supplementary Fig. S2). u Th s, fire-dependent sclerophyll Australia, the unique epicormic anatomy (types A and B: Supple- communities likely existed 50 million years before the well- mentary Table S1) of Myrtaceae, especially eucalypts, is known to 14–16 8,9,11 documented late-Miocene expansion of fire-dependent biomes . be responsible for post-fire recovery . Although scleromorphy We tested the hypothesis that protection of epicormic regenerative in the Australian flora dates back to the late Cretaceous , there tissue in Myrtaceae is positively correlated with flammability of is little direct charcoal fossil evidence for wildfire until the late habitat. Using phylogenetically independent contrasts, we found Miocene . Hence, it has been widely assumed that fire-dominated that these traits are correlated (Pagel94 maximum likelihood (ML) biomes became extensive only when the global climate aridified and 1,2,14 test, P = 0.027; Bayesian stochastic mapping test, P < 0.000001). became more seasonal aer ft 15 Ma . In other parts of the world, there is charcoal evidence that, in the lead-up to the Palaeocene– Biome transitions. We tested whether the variables in question are Eocene thermal maximum at 55 Ma, fire frequency increased , with phylogenetically conserved, because biome conservation has been global atmospheric oxygen levels above those of the present . During demonstrated previously in eucalypts , and conservation of post-fire this period, seasonally hot and dry climates originated both in nATuRE CommunICATIons | 2:193 | DoI: 10.1038/ncomms1191 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. nATuRE CommunICATIons | DoI: 10.1038/ncomms1191 ARTICLE 1.0 Vochysiaceae Psiloxyloideae 1.0 Xanthostemon 1.0 Lophostemon Osbornia 0.99 1.0 1.0 0.89 1.0 Melaleuceae 1.0 1.0 1.0 1.0 0.6 0.69 1.0 0.74 0.9 0.95 1.0 1.0 0.57 0.76 0.89 1.0 Myrteae 1.0 1.0 1.0 0.94 0.94 0.73 0.99 1.0 0.93 0.98 0.86 1.0 Lindsayomyrtus 0.85 1.0 0.85 Tristaniopsis 1.0 Backhousieae 1.0 0.58 0.78 0.98 1.0 1.0 1.0 0.61 1.0 1.0 Syzygieae 1.0 0.98 1.0 0.81 0.66 0.99 Tristanieae 1.0 1.0 0.67 1.0 1.0 Metrosidereae 1.0 1.0 Leptospermeae 1.0 0.57 1.0 1.0 1.0 1.0 0.52 1.0 0.95 0.61 Chamelaucieae 0.93 1.0 1.0 1.0 0.94 0.98 0.99 0.71 1.0 Syncarpia 1.0 Stockwellia clade 1.0 1.0 0.75 Eucalyptus 1.0 0.78 0.73 1.0 1.0 0.99 1.0 97 Corymbia 1.0 0.85 Angophora Arillastrum 80 70 60 50 40 30 20 10 0 Million years before present (Ma) Figure 1 | Inferred evolutionary history of post-fire epicormic resprouting mapped onto a Bayesian phylogeny of Myrtaceae. Time scale is millions of years before present (ma). Labels indicate higher taxa mentioned in the text. shading of boxes at tips indicates scoring for the trait ‘likely epicormic resprouter’ (black), ‘likely non-resprouter’ (white) or not scored (no box). Ancestral states reconstructed by parsimony are shown at internal branches; grey indicates an equivocal reconstruction. nodes labelled with upper case letters in circles are for reference from the text and tables. Decimal values on branches indicate Bayesian posterior probabilities; integers (in Corymbia) indicate parsimony bootstrap scores. nATuRE CommunICATIons | 2:193 | DoI: 10.1038/ncomms1191 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. ARTICLE nATuRE CommunICATIons | DoI: 10.1038/ncomms1191 1.0 Vochysiaceae Psiloxyloideae 1.0 G Xanthostemon F 1.0 Lophostemon Osbornia 0.99 1.0 1.0 0.89 1.0 Melaleuceae 1.0 1.0 1.0 1.0 0.6 0.69 1.0 0.74 0.9 0.95 1.0 1.0 0.57 0.76 0.89 1.0 Myrteae 1.0 1.0 1.0 U 0.94 0.94 0.73 0.99 1.0 0.93 0.98 0.86 1.0 Lindsayomyrtus 0.85 1.0 0.85 Tristaniopsis 1.0 Backhousieae 1.0 0.58 0.78 0.98 1.0 1.0 I 1.0 0.61 Syzygieae 1.0 1.0 1.0 0.98 1.0 0.81 0.66 0.99 1.0 Tristanieae 1.0 0.67 1.0 1.0 Metrosidereae 1.0 1.0 Leptospermeae 1.0 0.57 1.0 1.0 1.0 1.0 0.52 1.0 0.95 0.61 Chamelaucieae 0.93 1.0 1.0 1.0 0.94 0.98 0.99 0.71 1.0 L Syncarpia 1.0 Stockwellia clade 1.0 1.0 0.75 Eucalyptus 1.0 0.78 0.73 1.0 1.0 0.99 1.0 Corymbia 1.0 Angophora 0.85 Arillastrum 80 70 60 50 40 30 20 10 0 Million years before present (Ma) Figure 2 | Inferred evolutionary history of biome flammability mapped onto a Bayesian phylogeny of Myrtaceae. Time scale is millions of years before present (ma). Labels indicate higher taxa mentioned in the text. shading of boxes at tips and along branches indicates scoring for the trait ‘biome flammable’ (black) or ‘non-flammable’ (white). Ancestral states reconstructed by parsimony are shown at internal branches; grey indicates an equivocal reconstruction. nodes labelled with upper case letters in circles are for reference from the text and tables. Decimal values on branches indicate Bayesian posterior probabilities; integers (in Corymbia) indicate parsimony bootstrap scores. nATuRE CommunICATIons | 2:193 | DoI: 10.1038/ncomms1191 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. nATuRE CommunICATIons | DoI: 10.1038/ncomms1191 ARTICLE Table 1 | Estimated timing of transitions in epicormic and biome traits. Nodes (letter labels Age (median Ma Reconstructed as resprouter Reconstructed as flammable as in Figures) with 95% HPD*) Parsimony ML Shift period Parsimony ML Shift period state state† (Ma, 95% HPD*) state state† (Ma, 95% HPD*) A: myrtoideae crown 63 (61–65) no No — no No — Epicormic plus biome shifts Y: stem of 62 (60–64) no No — no No — Eucalypteae + Chamelaucieae + Leptospermeae‡,§ m: Crown of 60 (58–63) no No — Yes Yes — Eucalypteae + Chamelaucieae + Leptospermeae K: Eucalypteae + 60 (—) uncertain no — Yes Yes — syncarpieae C: Eucalyptinae 54 (52–57) Yes Yes 63–52 Yes Yes 63–58 D: Melaleuca + 50 (37–60) no no — no No — Osbornia‡ E: Melaleuca s.l. 34 (22–47) Yes Yes 60–22 Yes Yes 60–22 crown F: Xanthostemon + 48 (30–61) no No — no No — Lophostemon‡ G: Xanthostemon uncertain uncertain uncertain — no No — crown H: X. paradoxus 0 Yes Yes < 61 Yes Yes < 61 B: Eucalypteae‡,§ 57 (54–59) uncertain no — Yes Yes — Q: Stockwellia clade > 28 ( < 49) no No 59–10 no No 59–10 I: Tristaniopsis + 50 (41–59) no No — no No — Syzygium‡ J: Tristaniopsis crown < 34 ( < 49) Yes Yes 59–41 Yes Yes 59–41 Epicormic shifts, no biome shift Melaleuca < 34 ( < 47) no No < 47 Yes Yes no shift armillaris + M. hypericifolia Calothamnus < 34 ( < 47) no No < 47 Yes Yes no shift quadrifidus  Biome shift, no epicormic shift¶ Y: stem of 62 (60–64) no No — no No — Chamelaucieae + Leptospermeae + Eucalypteae‡,§ m: Crown of 61 (58–63) no No — Yes Yes — Chamelaucieae + Leptospermeae + Eucalypteae n: Chamelaucieae + 56 (54–58) no No no shift Yes Yes 54–64 Leptospermeae 32, *HPD is the Bayesian highest posterior density , equivalent to a 95% confidence interval. †mL is the maximum likelihood estimate of the preferred state. Entry given in bold indicates a significant preference from a likelihood ratio test ( P < 0.05). ‡This row represents the ancestral node and the following rows its descendants. §The sequence of events at the base of the eucalypts is unclear and the alternative reconstruction is described in the Results. Reversals to non-resprouting types within melaleuca, whose ancestor reconstructs as a resprouter occurring in the sclerophyll biome. The timing of these shifts is uncertain because of lack of branch length information within the group. ¶Also, in terminals Lophostemon lactifluus , Tristania neriifolia, Syzygium eucalyptoides, S. suborbiculare and Austromyrtus dulcis. All these transitions occurred ≤15 ma. 25 26 Australia and elsewhere , and such climates are characterized by the shifts into savanna inferred for Myrtaceae could have occurred fires ignited by electrical storms . Our results suggest, independently before 30 Ma, in the Oligocene or Eocene (Supplementary Fig. S2); of the fossil record, that fire-dominated communities were present however, all monsoonal lineages have long stems that terminate in Australia during this period. in the Miocene or even in the present. As a transition could have Limited palaeontological evidence suggests that a monsoonal occurred at any point along a lineage stem, none positively indicates 18,27 climate might have originated in Australia by 30 Ma . Some of a pre-Miocene origin of savanna (Supplementary Fig. S2). Multiple nATuRE CommunICATIons | 2:193 | DoI: 10.1038/ncomms1191 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. ARTICLE nATuRE CommunICATIons | DoI: 10.1038/ncomms1191 representation of their geography and biomes. Additionally, we sampled both lines of evidence show that the savanna biome expanded worldwide 15,16 genera of subfamily Psiloxyloideae and of the sister group, Vochysiaceae. in the late Miocene and our results for Myrtaceae are consistent e Th phylogeny was constructed in two stages. First, sequences of 111 taxa of with this. ITS (internal transcribed spacers of nuclear ribosomal DNA), matK and ndhF from Did the Myrtaceae make the flammable biomes or vice versa? Genbank (Supplementary Table S3) were aligned and concatenated ae ft r check - es Th e two alternatives make different predictions. If fire drove evo - ing for pseudogenes (ITS) and coni fl cts between data partitions. A rate-smoothed phylogeny, in which branch lengths were proportional to time (chronogram), was lutionary change, one might expect multiple consequent origins of derived using Bayesian inference in BEAST , ver. 1.5.4. e Th alignment was divided the trait that conveys tolerance. Alternatively, if the dominance of into seven partitions: ITS, 5′ a fl nking region of matK, r fi st codon sites of matK, Myrtaceae led to biome flammability, this could have resulted from second codon sites of matK, third codon sites of matK, r fi st codon sites of ndhF, a single preceding shift to epicormic resprouting in the family. Foliar second codon sites of ndhF and third codon sites of ndhF. Each partition was glands that produce aromatic oils are found throughout Myrtaceae, assigned an independent General Time Reversible model of nucleotide substitu- tion, chosen using the Bayesian information criterion, as calculated using Model- and probably evolved in their ancestor as a toxic defence against her- 28 generator . Rate variation among lineages was modelled using an uncorrelated bivores and also promoted flammability of plants . u Th s, epicormic lognormal relaxed clock and a birth–death process was used for the tree prior resprouting could be the result of selection originating as a by-product probability distribution. Posterior distributions of all parameter values, including of a defense system. However, our data show multiple origins of the tree, were estimated via Markov chain Monte Carlo (MCMC) sampling. r Th ee resprouting in Myrtaceae: once in each of Melaleuca, Tristaniopsis replicate MCMC runs were performed, with the tree and parameter values sampled 3 7 every 5×10 steps over a total of 5×10 steps. Tracer 1.5 (ref. 41) was used to assess and Xanthostemon and once or twice in the eucalypt–Syncarpia convergence between runs and to estimate an appropriate number of samples lineage (Fig. 1), favouring the hypothesis that flammable biomes to discard as burn-in by ensuring that ee ff ctive sample sizes were suc ffi ient (that originated first. er Th e is no evidence that the epicormic change pre - is, > 200) to provide reasonable estimates of model parameter variance. i Th s was ceded the shift to a flammable biome in any lineage; rather, the biome done by progressively discarding samples until all ee ff ctive sample sizes exceeded transition apparently occurred before the epicormic change in the 200. Posterior samples from the three independent runs were combined and the trees and parameter values were summarized. e Th sampled tree with the maximum eucalypt–Syncarpia lineage (see, Supplementary Figs S1 and S2). product of clade credibilities was identie fi d using TreeAnnotator and viewed using A third possibility combines these scenarios. Myrtaceae could have FigTree 1.3.1 (ref. 42). e Th phylogeny was estimated both with and without internal risen to dominance first, favouring a fire regime that then selected constraints to test whether calibration ae ff cted the topology . for epicormic shifts in multiple lineages, thus initiating a feedback Calibration of the relaxed molecular clock. To estimate absolute divergence loop that maintained or increased the dominance of Myrtaceae. times, the analysis was calibrated using pollen fossils of known age placed at e Th eucalypts appear to be the key to the rise to dominance of the seven internal nodes. Fossil pollens suitable for calibration were identified using Myrtaceae in Australia. Why then have eucalypts not taken over the a backbone-constraint test . This method searches for the most parsimonious seasonally dry regions of the world? During the Miocene, eucalypts placement of fossil pollens on a molecular phylogeny, using a pollen character data were present in New Zealand and Southeast Asia in association with matrix scored for the terminal taxa. A total of 26 pollen fossils were added one at a time to a morphological matrix containing 111 extant taxa and 11 pollen char- other sclerophyll and xeric flora, such as acacias, chenopods and 7,29,30 acters. The phylogenetic placement of each fossil on the unconstrained molecular Casuarinaceae . At this time, there was an abundance of char- phylogeny was estimated using heuristic parsimony searches of 100 random-addi- 29,30 coal, indicating frequent burning in these communities . Multiple tion replicates with tree-bisection-reconnection in PAUP* , with the tree-search crown-group eucalypt lineages were also present in Patagonia dur- constrained by the molecular phylogeny estimated without internal calibrations. ing the early Eocene . e Th y persist in Southeast Asia today, but have As suggested , the most parsimonious + 1 and + 2 trees were also saved, to assess confidence of fossil placements. The test identified seven fossils as suitable for since gone extinct in New Zealand and Patagonia, likely as a result calibration (Supplementary Table S2). In cases in which more than one fossil was of climate change to wetter and colder conditions that are no longer placed at a given node, the oldest was used for calibration. Nodes used as calibra- 19,32 so prone to fire . Dispersal limitation may account for the lack of tion points (Supplementary Table S2) were constrained to be monophyletic in the spread of eucalypts beyond the immediate region since the end of BEAST analysis; all these nodes were supported in the unconstrained analysis. the Eocene, when Australia separated from East Gondwana. A prior distribution (lognormal or normal) was assigned to each calibration point, as recommended . The root of the tree, being the stem node of Myrtaceae, Recently, it was suggested that eucalypts could make a large was calibrated with a normally distributed age estimate of 85 Ma with s.d. = 2.5 contribution to carbon sequestration in a future greenhouse world, (Supplementary Table S2). We used the fossil Myrtaceidites mesonesus (61 Ma) to based on a demonstrated positive growth response to an elevation calibrate the crown of Myrtaceae instead of M. lisamae (~86 Ma), used previously , of either atmospheric CO or temperature . Our results independ- 2 because the backbone-constraint test indicated that the latter was probably mis- ently predict that eucalypt forests and woodlands could be a supe- placed as a member of the Myrtaceae crown. Recently, 52-Ma Eucalyptus macrofos- sils were discovered in Patagonia and are older than our 37 Ma constraint rior long-term carbon bank compared with climatically similar (M. eucalyptoides, Supplementary Table S2) for the crown node of the genus. fire-dependent biomes in other continents. By resprouting from the However, we could not use the Patagonian fossils as a constraint because morpho- trunk and branches, eucalypts preserve most of their aboveground logical descriptions needed to place them on the phylogeny are not yet published. woody biomass aer ft wildfires, both in northern savanna and in If we had been able to use these fossils as a constraint, our dating estimates could sclerophyll forest of the temperate southeast . In contrast, other have been even older, implying even earlier origins of flammability. trees that do not resprout epicormically lose their aerial wood aer ft Interpolation of taxa with known anatomy. In the second stage of the phylo- high-intensity fire (as opposed to lower-intensity fires, which their genetics, 52 taxa with known epicormic anatomy (Supplementary Table S1), but stems might survive). Consequently, in non-epicormic resprouters, lacking sequence data, were interpolated by hand into the chronogram (Figs 1 and 2; the woody biomass decays and the stored carbon is released aer ft Supplementary Figs S1 and S2) on the basis of their position in other phylogenies, 27,46,47 48 49 the fire. Such trees either resprout from the base or are killed and that is, eucalypts , Melaleuca , Syzygium s.l. and Myrtaceae, using matK 35,36 only . Chronological branch lengths were unavailable for some interpolated taxa regenerate from seed . e Th y recover more slowly than eucalypts 37 and, in these cases, branch lengths were arbitrarily equalized above and below aer ft fire and are forced to accumulate aboveground wood from the interpolated nodes. This did not ae ff ct the inferences of trait evolution in the scratch. When a pine forest planted for carbon capture burns, the eucalypt lineage because the transitions to flammability occurred near the base of trees die and the carbon bank drains. the tree, where branch length information was available. However, branch length uncertainty within Syncarpia, Tristaniopsis and Xanthostemon resulted in wide bounds on the timing estimates of transitions within these lineages (Table 1). Methods Phylogenetics. A dated molecular phylogeny of Myrtaceae was constructed using 66 species with known epicormic anatomy (Supplementary Table S1) and 97 Epicormic anatomy. We scored a matrix for five epicormic structural types 8–11,50 additional taxa, totalling 163 terminals representing higher taxa across the family, across 66 myrtaceous taxa studied to date and for their biome of occurrence on the basis of a recent phylogenetic classification of the family . Most deep-level (Supplementary Table S1). In the first (type A), the bud-forming cells comprise phylogenetic diversity in the family is found within Australia (for example, 14 of meristem strips (that is, radially oriented strips of cells of meristematic appear- 15 tribes in subfamily Myrtoideae), but we also sampled extra-Australian members ance) and are present at all depths in the bark, and in most cases probably extend a of these (where applicable) and the sixteenth tribe (Metrosidereae) to ensure short distance into the outer secondary xylem. For the available bark thickness, this nATuRE CommunICATIons | 2:193 | DoI: 10.1038/ncomms1191 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. nATuRE CommunICATIons | DoI: 10.1038/ncomms1191 ARTICLE structure provides the maximum heat protection for the bud-forming cells. In the 9. Burrows, G. E. Syncarpia and Tristaniopsis (Myrtaceae) possess specialised fire- second type (B), the epicormic buds or bud-forming meristems are located close resistant epicormic structures. Aust. J. Bot. 56, 254–264 (2008). to the cambial surface and covered by numerous layers of dead bark (paperbarks). 10. Waters, D. A., Burrows, G. E. & Harper, J. D. I. Eucalyptus regnans (Myrtaceae): e p Th apery structure provides maximum heat protection for the bud-forming a fire-sensitive eucalypt with a resprouter epicormic structure. Am. J. Bot. 97, cells, but buds need to emerge through numerous bark layers. In the third type (C), 545–556 (2010). epicormic buds are located at the base of a narrow depression in the bark and are 11. Burrows, G. E. et al. A wide diversity of epicormic structures is present in thus about halfway between the bark surface and the cambial surface. This provides Myrtaceae species in the northern Australian savanna biome—implications for an intermediate level of protection for the available bark thickness. In the fourth adaptation to fire. Aust. J. Bot. 58, 493–507 (2010). type (D), epicormic buds are situated at or near the bark surface, giving minimal 12. Fink, S. The occurrence of adventitious and preventitious buds within the bark protection from the heat of a fire. In the fifth type (E), epicormic bud-forming of some temperate and tropical trees. Am. J. Bot. 70, 532–542 (1983). structures are apparently absent. Various processes have been implicated in the 13. Orians, G. H. & Milewski, A. V. Ecology of Australia: the effects of nutrient- death of epicormic buds or failure in their initial development . poor soils and intense fires. Biol. Rev. 82, 393–423 (2007). 14. Kershaw, A. P., Clark, J. S., Gill, A. M. & D’Costa, D. M. In Flammable Australia: Trait evolution. These data were imported into Mesquite ver. 2.7 (ref. 51) and e Th Fire Regimes and Biodiversity of Australia (eds Bradstock, R. A., Williams, J. E. SIMMAP ver. 1.5 (ref. 52) together with the phylogeny constructed as above. & Gill, M. A.) 3–25 (Cambridge Univ. Press, 2002). Some of the statistical tests used in Mesquite required binary variables; hence, the 15. Bond, W. J. What limits trees in C-4 grasslands and savannas? Annu. Rev. Ecol. epicormic character was rescored to indicate whether the anatomy of each species Evol. Syst. 39, 641–659 (2008). indicated a likely (types A–C) or unlikely (types D and E) epicormic resprouter 16. Beerling, D. J. & Osborne, C. P. The origin of the savanna biome. 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G.E.B. contributed the epicormic anatomy data and interpretation for scoring. A.H.T. Higher-level relationships among the eucalypts are resolved by ITS sequence contributed the sequence and calibration data and did the Bayesian phylogenetic data. Aust. Syst. Bot. 15, 49–62 (2002). analysis. D.M.J.S.B. conceived the study and provided background information on fire 47. Steane, D. A., Nicolle, D. & Potts, B. M. Phylogenetic positioning of anomalous ecology. M.D.C. made the final phylogeny, performed the trait evolution analyses and eucalypts by using ITS sequence data. Aust. Syst. Bot. 20, 402–408 wrote the manuscript in collaboration with L.G.C. All authors discussed the results and (2007). commented on the manuscript. 48. Edwards, R. D., Craven, L. A., Crisp, M. D. & Cook, L. G. Melaleuca revisited: cpDNA data confirm that Melaleuca L. (Myrtaceae) is not monophyletic. Taxon 59, 744–754 (2010). Additional information 49. Biffin, E. et al. Evolution of exceptional species richness amongst lineages of Supplementary Information accompanies this paper at http://www.nature.com/ fleshy-fruited Myrtaceae. Ann. Bot. 106, 79–93 (2010). naturecommunications 50. Burrows, G. E. An anatomical study of epicormic bud strand structure in Eucalyptus cladocalyx (Myrtaceae). Aust. J. Bot. 48, 233–245 (2000). Competing financial interests: The authors declare no competing financial interests. 51. Maddison, W. P. & Maddison, D. R. Mesquite: a modular system for Reprints and permission information is available online at http://npg.nature.com/ evolutionary analysis. Version 2.7., http://mesquiteproject.org (2009). reprintsandpermissions/ 52. Bollback, J. P. SIMMAP: Stochastic character mapping of discrete traits on How to cite this article: Crisp, M. D. et al. Flammable biomes dominated by phylogenies. BMC Bioinf. 7, 88 (2006). 53. Lewis, P. O. A likelihood approach to estimating phylogeny from discrete eucalypts originated at the Cretaceous–Palaeogene boundary. Nat. Commun. 2:193 morphological character data. Syst. Biol. 50, 913–925 (2001). doi: 10.1038/ncomms1191 (2011). nATuRE CommunICATIons | 2:193 | DoI: 10.1038/ncomms1191 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Nature Communications Springer Journals

Flammable biomes dominated by eucalypts originated at the Cretaceous–Palaeogene boundary

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Copyright © 2011 by Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.
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Science, Humanities and Social Sciences, multidisciplinary; Science, Humanities and Social Sciences, multidisciplinary; Science, multidisciplinary
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Abstract

ARTICLE DOI: 10.1038/ncomms1191 Received 20 may 2010 | Accepted 12 Jan 2011 | Published 15 Feb 2011 Flammable biomes dominated by eucalypts originated at the Cretaceous–Palaeogene boundary 1 2 3 1 4 michael D. Crisp , Geoffrey E. Burrows , Lyn G. Cook , Andrew H. Thornhill & David m. J. s. Bowman Fire is a major modifier of communities, but the evolutionary origins of its prevalent role in shaping current biomes are uncertain. Australia is among the most fire-prone continents, with most of the landmass occupied by the fire-dependent sclerophyll and savanna biomes. In contrast to biomes with similar climates in other continents, Australia has a tree flora dominated by a single genus, Eucalyptus, and related myrtaceae. A unique mechanism in myrtaceae for enduring and recovering from fire damage likely resulted in this dominance. Here, we find a conserved phylogenetic relationship between post-fire resprouting (epicormic) anatomy and biome evolution, dating from 60 to 62 ma, in the earliest Palaeogene. Thus, fire-dependent communities likely existed 50 million years earlier than previously thought. We predict that epicormic resprouting could make eucalypt forests and woodlands an excellent long-term carbon bank for reducing atmospheric Co compared with biomes with similar fire regimes in other continents. Division of Evolution, Ecology and Genetics, Research School of Biology, The Australian National University, Canberra, Australian Capital Territory 0200, 2 3 Australia. Institute for Land, Water and Society, Charles Sturt University, Locked Bag 588, Wagga Wagga, New South Wales 2678, Australia. School of Biological Sciences, The University of Queensland, Brisbane, Queensland 4072, Australia. School of Plant Science, Private Bag, Hobart, Tasmania 7001, Australia. Correspondence and requests for materials should be addressed to M.D.C. (email: mike.crisp@anu.edu.au). nATuRE CommunICATIons | 2:193 | DoI: 10.1038/ncomms1191 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. ARTICLE nATuRE CommunICATIons | DoI: 10.1038/ncomms1191 pen-canopied communities are far more extensive across persistence traits has been found in taxa occurring in fire-dependent the world than predicted by consideration of climate and communities. Biome adaptations in the Myrtaceae are significantly Osoil fertility alone . Moreover, boundaries between open conserved (tip randomization test, P < 0.001) and the transitions woodlands and closed-canopy rainforest are oen ft surprisingly that have occurred are strongly directional—all sclerophyll lineages 1,2 sharp . Fire is known to have a major role in maintaining open originated from a rainforest ancestor and all monsoonal savanna communities: both plot experiments and modelling show that, in the lineages arose more recently, from sclerophyll or rainforest ances- 2,3 absence of fire, closed forests would cover much of both Australia tors. Two-thirds (21) of biome shifts were into savanna, confirming 1 1 and the world —hence their definition as ‘fire-dependent’ . In that this biome is a sink relative to the other biomes and suggest- Australia this effect is extreme, with rainforest marginalized by fire ing that the advent of monsoonal climate opened a major ecologi- to a tiny portion (2%) of the continent and absent from much of cal opportunity that pre-adapted Myrtaceae were able to exploit the climatically and edaphically suitable landscape . Even the vast effectively. However, we found no support for the hypothesis that 4,5 central Australian arid zone is dominated by fire at frequencies this new environment (with its more frequent but less intense 6,18 similar to those in temperate grassy woodlands and dry sclerophyll fires ) exerted sufficient selection to alter the epicormic anatomy 6 1 forests (global modelling suggesting that this region is ‘bare’ is of the Myrtaceae overall (Pagel94 ML test, P = 0.137; Bayesian simplistic). In contrast with other continents, a single diverse family, stochastic mapping test, P = 0.2), except in Xanthostemon and Myrtaceae, dominates Australian fire-dependent woodlands and perhaps Melaleuca (Supplementary Fig. S1). By contrast, v fi e of the forests, with 1,600 species, including 800 eucalypts and their close seven transitions in epicormic resprouting anatomy coincided with relatives . Many are excellent post-fire epicormic resprouters from shifts between the everwet and sclerophyll biomes ( Table 1). 8–11 the stems and branches aer ft high-intensity fires . In most investi- gated angiosperm trees, dormant epicormic buds are situated in the Alternative reconstructions. e Th sequence of events at the base of 8,12 outer bark , where they are likely killed by fire, but in eucalypts, the eucalypts is unclear because of uncertain trait reconstructions at the epicormic bud-forming structures are located deeply, where nodes M and K (Figs 1 and 2; Supplementary Figs S1 and S2) and they are protected by the full thickness of the bark and can sprout lack of support for the position of Syncarpia. e Th inferred trait tran - even aer ft high-intensity fires . Moreover, the epicormic structures sitions shown in Table 1 are a shift into the sclerophyll biome with a of eucalypts appear unique, consisting not of buds but of narrow, gain of resprouting epicormic type A between nodes Y and K, and a radially oriented strips of cells of meristematic appearance, and as reversal of both traits in the Stockwellia clade (node Q). e Th alterna - 8–11 such differ from those recorded in other families . tive reconstruction infers an independent transition to sclerophyll Given the above, it has been hypothesized that evolution of fire and epicormic resprouting in each of Syncarpia and Eucalypteae, tolerance in Myrtaceae was directly linked with the origins and with retention of the ancestral everwet biome and epicormic res- expansion of the fire-dependent biomes in Australia, especially the prouting in the Stockwellia clade. e Th timing of these alternative 2,6,13 southern sclerophyll and northern savanna biomes . However, the reconstructions (62–55 Ma) is about the same as in the reconstruc- influence of wildfire on the evolution of Australian biomes through tions shown in the Figures and Table 1. e Th lack of branch length the Palaeogene, when Australia was still part of East Gondwana, has data for interpolated species within Syncarpia, Tristaniopsis and been little studied. e Th Australian fossil record has provided little Xanthostemon resulted in wide bounds on the timing estimates direct evidence of fire (fusain charcoal) before the mid-Miocene, of transitions within these lineages (Table 1). Reversals to non- when the climate aridified and charcoal levels increased dramati - resprouting types occurred within Melaleuca, whose most recent 2,14 cally . Here, we show that specialized epicormic resprouting origi- common ancestor reconstructs as a resprouter occurring in the nated in the eucalypt lineage much earlier, at least 60 million years sclerophyll biome. e Th timing of these shifts is uncertain because of ago. We find a significant link between the evolution of this unique lack of branch length information within the group. anatomy and the timing of shifts by Myrtaceae into the flammable sclerophyll biome. However, there was no statistical association with Discussion the more recent shifts into the monsoonal biome, which experiences We have shown that both epicormic resprouting in Myrtaceae more frequent but less intense fires. Our results contrast with the and flammable sclerophyll biomes likely originated in the earliest current view that fire-dominated vegetation originated much later, Cenozoic, 60–62 Ma, and that their evolution is significantly linked. aer ft global climate aridified and the monsoonal biome developed, In eucalypts, the distinctive epicormic resprouting anatomy has 14–16 in the late Miocene . been strictly conserved until the present, despite changes in habitat and response to fire. For example, Eucalyptus brachyandra grows on Results fire-protected cliffs and E. regnans dominates wet sclerophyll for- Ancestral biomes and epicormic structures. Using trait mapping est and, although usually killed by high-intensity fires, still retains on a dated molecular phylogeny, we found that both epicormic capacity to resprout epicormically aer les ft s intense fires . resprouting in Myrtaceae and their adaptation to the sclerophyll Sclerophyllous morphology is oen ft assumed to be an adapta - 13,19,20 biome probably evolved in the earliest Palaeogene, 60–62 Ma (Figs 1 tion to fire and a driver of diversification , but sclerophylly has and 2; Table 1; Supplementary Figs S1 and S2). e Th myrtoid ancestor diverse functions and is not necessarily an indicator of climates in 2,21,22 reconstructs as a non-resprouting inhabitant of rainforest (Table 1; general or fire-prone vegetation in particular . Nevertheless, in Fig. 1; Supplementary Fig. S2). u Th s, fire-dependent sclerophyll Australia, the unique epicormic anatomy (types A and B: Supple- communities likely existed 50 million years before the well- mentary Table S1) of Myrtaceae, especially eucalypts, is known to 14–16 8,9,11 documented late-Miocene expansion of fire-dependent biomes . be responsible for post-fire recovery . Although scleromorphy We tested the hypothesis that protection of epicormic regenerative in the Australian flora dates back to the late Cretaceous , there tissue in Myrtaceae is positively correlated with flammability of is little direct charcoal fossil evidence for wildfire until the late habitat. Using phylogenetically independent contrasts, we found Miocene . Hence, it has been widely assumed that fire-dominated that these traits are correlated (Pagel94 maximum likelihood (ML) biomes became extensive only when the global climate aridified and 1,2,14 test, P = 0.027; Bayesian stochastic mapping test, P < 0.000001). became more seasonal aer ft 15 Ma . In other parts of the world, there is charcoal evidence that, in the lead-up to the Palaeocene– Biome transitions. We tested whether the variables in question are Eocene thermal maximum at 55 Ma, fire frequency increased , with phylogenetically conserved, because biome conservation has been global atmospheric oxygen levels above those of the present . During demonstrated previously in eucalypts , and conservation of post-fire this period, seasonally hot and dry climates originated both in nATuRE CommunICATIons | 2:193 | DoI: 10.1038/ncomms1191 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. nATuRE CommunICATIons | DoI: 10.1038/ncomms1191 ARTICLE 1.0 Vochysiaceae Psiloxyloideae 1.0 Xanthostemon 1.0 Lophostemon Osbornia 0.99 1.0 1.0 0.89 1.0 Melaleuceae 1.0 1.0 1.0 1.0 0.6 0.69 1.0 0.74 0.9 0.95 1.0 1.0 0.57 0.76 0.89 1.0 Myrteae 1.0 1.0 1.0 0.94 0.94 0.73 0.99 1.0 0.93 0.98 0.86 1.0 Lindsayomyrtus 0.85 1.0 0.85 Tristaniopsis 1.0 Backhousieae 1.0 0.58 0.78 0.98 1.0 1.0 1.0 0.61 1.0 1.0 Syzygieae 1.0 0.98 1.0 0.81 0.66 0.99 Tristanieae 1.0 1.0 0.67 1.0 1.0 Metrosidereae 1.0 1.0 Leptospermeae 1.0 0.57 1.0 1.0 1.0 1.0 0.52 1.0 0.95 0.61 Chamelaucieae 0.93 1.0 1.0 1.0 0.94 0.98 0.99 0.71 1.0 Syncarpia 1.0 Stockwellia clade 1.0 1.0 0.75 Eucalyptus 1.0 0.78 0.73 1.0 1.0 0.99 1.0 97 Corymbia 1.0 0.85 Angophora Arillastrum 80 70 60 50 40 30 20 10 0 Million years before present (Ma) Figure 1 | Inferred evolutionary history of post-fire epicormic resprouting mapped onto a Bayesian phylogeny of Myrtaceae. Time scale is millions of years before present (ma). Labels indicate higher taxa mentioned in the text. shading of boxes at tips indicates scoring for the trait ‘likely epicormic resprouter’ (black), ‘likely non-resprouter’ (white) or not scored (no box). Ancestral states reconstructed by parsimony are shown at internal branches; grey indicates an equivocal reconstruction. nodes labelled with upper case letters in circles are for reference from the text and tables. Decimal values on branches indicate Bayesian posterior probabilities; integers (in Corymbia) indicate parsimony bootstrap scores. nATuRE CommunICATIons | 2:193 | DoI: 10.1038/ncomms1191 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. ARTICLE nATuRE CommunICATIons | DoI: 10.1038/ncomms1191 1.0 Vochysiaceae Psiloxyloideae 1.0 G Xanthostemon F 1.0 Lophostemon Osbornia 0.99 1.0 1.0 0.89 1.0 Melaleuceae 1.0 1.0 1.0 1.0 0.6 0.69 1.0 0.74 0.9 0.95 1.0 1.0 0.57 0.76 0.89 1.0 Myrteae 1.0 1.0 1.0 U 0.94 0.94 0.73 0.99 1.0 0.93 0.98 0.86 1.0 Lindsayomyrtus 0.85 1.0 0.85 Tristaniopsis 1.0 Backhousieae 1.0 0.58 0.78 0.98 1.0 1.0 I 1.0 0.61 Syzygieae 1.0 1.0 1.0 0.98 1.0 0.81 0.66 0.99 1.0 Tristanieae 1.0 0.67 1.0 1.0 Metrosidereae 1.0 1.0 Leptospermeae 1.0 0.57 1.0 1.0 1.0 1.0 0.52 1.0 0.95 0.61 Chamelaucieae 0.93 1.0 1.0 1.0 0.94 0.98 0.99 0.71 1.0 L Syncarpia 1.0 Stockwellia clade 1.0 1.0 0.75 Eucalyptus 1.0 0.78 0.73 1.0 1.0 0.99 1.0 Corymbia 1.0 Angophora 0.85 Arillastrum 80 70 60 50 40 30 20 10 0 Million years before present (Ma) Figure 2 | Inferred evolutionary history of biome flammability mapped onto a Bayesian phylogeny of Myrtaceae. Time scale is millions of years before present (ma). Labels indicate higher taxa mentioned in the text. shading of boxes at tips and along branches indicates scoring for the trait ‘biome flammable’ (black) or ‘non-flammable’ (white). Ancestral states reconstructed by parsimony are shown at internal branches; grey indicates an equivocal reconstruction. nodes labelled with upper case letters in circles are for reference from the text and tables. Decimal values on branches indicate Bayesian posterior probabilities; integers (in Corymbia) indicate parsimony bootstrap scores. nATuRE CommunICATIons | 2:193 | DoI: 10.1038/ncomms1191 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. nATuRE CommunICATIons | DoI: 10.1038/ncomms1191 ARTICLE Table 1 | Estimated timing of transitions in epicormic and biome traits. Nodes (letter labels Age (median Ma Reconstructed as resprouter Reconstructed as flammable as in Figures) with 95% HPD*) Parsimony ML Shift period Parsimony ML Shift period state state† (Ma, 95% HPD*) state state† (Ma, 95% HPD*) A: myrtoideae crown 63 (61–65) no No — no No — Epicormic plus biome shifts Y: stem of 62 (60–64) no No — no No — Eucalypteae + Chamelaucieae + Leptospermeae‡,§ m: Crown of 60 (58–63) no No — Yes Yes — Eucalypteae + Chamelaucieae + Leptospermeae K: Eucalypteae + 60 (—) uncertain no — Yes Yes — syncarpieae C: Eucalyptinae 54 (52–57) Yes Yes 63–52 Yes Yes 63–58 D: Melaleuca + 50 (37–60) no no — no No — Osbornia‡ E: Melaleuca s.l. 34 (22–47) Yes Yes 60–22 Yes Yes 60–22 crown F: Xanthostemon + 48 (30–61) no No — no No — Lophostemon‡ G: Xanthostemon uncertain uncertain uncertain — no No — crown H: X. paradoxus 0 Yes Yes < 61 Yes Yes < 61 B: Eucalypteae‡,§ 57 (54–59) uncertain no — Yes Yes — Q: Stockwellia clade > 28 ( < 49) no No 59–10 no No 59–10 I: Tristaniopsis + 50 (41–59) no No — no No — Syzygium‡ J: Tristaniopsis crown < 34 ( < 49) Yes Yes 59–41 Yes Yes 59–41 Epicormic shifts, no biome shift Melaleuca < 34 ( < 47) no No < 47 Yes Yes no shift armillaris + M. hypericifolia Calothamnus < 34 ( < 47) no No < 47 Yes Yes no shift quadrifidus  Biome shift, no epicormic shift¶ Y: stem of 62 (60–64) no No — no No — Chamelaucieae + Leptospermeae + Eucalypteae‡,§ m: Crown of 61 (58–63) no No — Yes Yes — Chamelaucieae + Leptospermeae + Eucalypteae n: Chamelaucieae + 56 (54–58) no No no shift Yes Yes 54–64 Leptospermeae 32, *HPD is the Bayesian highest posterior density , equivalent to a 95% confidence interval. †mL is the maximum likelihood estimate of the preferred state. Entry given in bold indicates a significant preference from a likelihood ratio test ( P < 0.05). ‡This row represents the ancestral node and the following rows its descendants. §The sequence of events at the base of the eucalypts is unclear and the alternative reconstruction is described in the Results. Reversals to non-resprouting types within melaleuca, whose ancestor reconstructs as a resprouter occurring in the sclerophyll biome. The timing of these shifts is uncertain because of lack of branch length information within the group. ¶Also, in terminals Lophostemon lactifluus , Tristania neriifolia, Syzygium eucalyptoides, S. suborbiculare and Austromyrtus dulcis. All these transitions occurred ≤15 ma. 25 26 Australia and elsewhere , and such climates are characterized by the shifts into savanna inferred for Myrtaceae could have occurred fires ignited by electrical storms . Our results suggest, independently before 30 Ma, in the Oligocene or Eocene (Supplementary Fig. S2); of the fossil record, that fire-dominated communities were present however, all monsoonal lineages have long stems that terminate in Australia during this period. in the Miocene or even in the present. As a transition could have Limited palaeontological evidence suggests that a monsoonal occurred at any point along a lineage stem, none positively indicates 18,27 climate might have originated in Australia by 30 Ma . Some of a pre-Miocene origin of savanna (Supplementary Fig. S2). Multiple nATuRE CommunICATIons | 2:193 | DoI: 10.1038/ncomms1191 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. ARTICLE nATuRE CommunICATIons | DoI: 10.1038/ncomms1191 representation of their geography and biomes. Additionally, we sampled both lines of evidence show that the savanna biome expanded worldwide 15,16 genera of subfamily Psiloxyloideae and of the sister group, Vochysiaceae. in the late Miocene and our results for Myrtaceae are consistent e Th phylogeny was constructed in two stages. First, sequences of 111 taxa of with this. ITS (internal transcribed spacers of nuclear ribosomal DNA), matK and ndhF from Did the Myrtaceae make the flammable biomes or vice versa? Genbank (Supplementary Table S3) were aligned and concatenated ae ft r check - es Th e two alternatives make different predictions. If fire drove evo - ing for pseudogenes (ITS) and coni fl cts between data partitions. A rate-smoothed phylogeny, in which branch lengths were proportional to time (chronogram), was lutionary change, one might expect multiple consequent origins of derived using Bayesian inference in BEAST , ver. 1.5.4. e Th alignment was divided the trait that conveys tolerance. Alternatively, if the dominance of into seven partitions: ITS, 5′ a fl nking region of matK, r fi st codon sites of matK, Myrtaceae led to biome flammability, this could have resulted from second codon sites of matK, third codon sites of matK, r fi st codon sites of ndhF, a single preceding shift to epicormic resprouting in the family. Foliar second codon sites of ndhF and third codon sites of ndhF. Each partition was glands that produce aromatic oils are found throughout Myrtaceae, assigned an independent General Time Reversible model of nucleotide substitu- tion, chosen using the Bayesian information criterion, as calculated using Model- and probably evolved in their ancestor as a toxic defence against her- 28 generator . Rate variation among lineages was modelled using an uncorrelated bivores and also promoted flammability of plants . u Th s, epicormic lognormal relaxed clock and a birth–death process was used for the tree prior resprouting could be the result of selection originating as a by-product probability distribution. Posterior distributions of all parameter values, including of a defense system. However, our data show multiple origins of the tree, were estimated via Markov chain Monte Carlo (MCMC) sampling. r Th ee resprouting in Myrtaceae: once in each of Melaleuca, Tristaniopsis replicate MCMC runs were performed, with the tree and parameter values sampled 3 7 every 5×10 steps over a total of 5×10 steps. Tracer 1.5 (ref. 41) was used to assess and Xanthostemon and once or twice in the eucalypt–Syncarpia convergence between runs and to estimate an appropriate number of samples lineage (Fig. 1), favouring the hypothesis that flammable biomes to discard as burn-in by ensuring that ee ff ctive sample sizes were suc ffi ient (that originated first. er Th e is no evidence that the epicormic change pre - is, > 200) to provide reasonable estimates of model parameter variance. i Th s was ceded the shift to a flammable biome in any lineage; rather, the biome done by progressively discarding samples until all ee ff ctive sample sizes exceeded transition apparently occurred before the epicormic change in the 200. Posterior samples from the three independent runs were combined and the trees and parameter values were summarized. e Th sampled tree with the maximum eucalypt–Syncarpia lineage (see, Supplementary Figs S1 and S2). product of clade credibilities was identie fi d using TreeAnnotator and viewed using A third possibility combines these scenarios. Myrtaceae could have FigTree 1.3.1 (ref. 42). e Th phylogeny was estimated both with and without internal risen to dominance first, favouring a fire regime that then selected constraints to test whether calibration ae ff cted the topology . for epicormic shifts in multiple lineages, thus initiating a feedback Calibration of the relaxed molecular clock. To estimate absolute divergence loop that maintained or increased the dominance of Myrtaceae. times, the analysis was calibrated using pollen fossils of known age placed at e Th eucalypts appear to be the key to the rise to dominance of the seven internal nodes. Fossil pollens suitable for calibration were identified using Myrtaceae in Australia. Why then have eucalypts not taken over the a backbone-constraint test . This method searches for the most parsimonious seasonally dry regions of the world? During the Miocene, eucalypts placement of fossil pollens on a molecular phylogeny, using a pollen character data were present in New Zealand and Southeast Asia in association with matrix scored for the terminal taxa. A total of 26 pollen fossils were added one at a time to a morphological matrix containing 111 extant taxa and 11 pollen char- other sclerophyll and xeric flora, such as acacias, chenopods and 7,29,30 acters. The phylogenetic placement of each fossil on the unconstrained molecular Casuarinaceae . At this time, there was an abundance of char- phylogeny was estimated using heuristic parsimony searches of 100 random-addi- 29,30 coal, indicating frequent burning in these communities . Multiple tion replicates with tree-bisection-reconnection in PAUP* , with the tree-search crown-group eucalypt lineages were also present in Patagonia dur- constrained by the molecular phylogeny estimated without internal calibrations. ing the early Eocene . e Th y persist in Southeast Asia today, but have As suggested , the most parsimonious + 1 and + 2 trees were also saved, to assess confidence of fossil placements. The test identified seven fossils as suitable for since gone extinct in New Zealand and Patagonia, likely as a result calibration (Supplementary Table S2). In cases in which more than one fossil was of climate change to wetter and colder conditions that are no longer placed at a given node, the oldest was used for calibration. Nodes used as calibra- 19,32 so prone to fire . Dispersal limitation may account for the lack of tion points (Supplementary Table S2) were constrained to be monophyletic in the spread of eucalypts beyond the immediate region since the end of BEAST analysis; all these nodes were supported in the unconstrained analysis. the Eocene, when Australia separated from East Gondwana. A prior distribution (lognormal or normal) was assigned to each calibration point, as recommended . The root of the tree, being the stem node of Myrtaceae, Recently, it was suggested that eucalypts could make a large was calibrated with a normally distributed age estimate of 85 Ma with s.d. = 2.5 contribution to carbon sequestration in a future greenhouse world, (Supplementary Table S2). We used the fossil Myrtaceidites mesonesus (61 Ma) to based on a demonstrated positive growth response to an elevation calibrate the crown of Myrtaceae instead of M. lisamae (~86 Ma), used previously , of either atmospheric CO or temperature . Our results independ- 2 because the backbone-constraint test indicated that the latter was probably mis- ently predict that eucalypt forests and woodlands could be a supe- placed as a member of the Myrtaceae crown. Recently, 52-Ma Eucalyptus macrofos- sils were discovered in Patagonia and are older than our 37 Ma constraint rior long-term carbon bank compared with climatically similar (M. eucalyptoides, Supplementary Table S2) for the crown node of the genus. fire-dependent biomes in other continents. By resprouting from the However, we could not use the Patagonian fossils as a constraint because morpho- trunk and branches, eucalypts preserve most of their aboveground logical descriptions needed to place them on the phylogeny are not yet published. woody biomass aer ft wildfires, both in northern savanna and in If we had been able to use these fossils as a constraint, our dating estimates could sclerophyll forest of the temperate southeast . In contrast, other have been even older, implying even earlier origins of flammability. trees that do not resprout epicormically lose their aerial wood aer ft Interpolation of taxa with known anatomy. In the second stage of the phylo- high-intensity fire (as opposed to lower-intensity fires, which their genetics, 52 taxa with known epicormic anatomy (Supplementary Table S1), but stems might survive). Consequently, in non-epicormic resprouters, lacking sequence data, were interpolated by hand into the chronogram (Figs 1 and 2; the woody biomass decays and the stored carbon is released aer ft Supplementary Figs S1 and S2) on the basis of their position in other phylogenies, 27,46,47 48 49 the fire. Such trees either resprout from the base or are killed and that is, eucalypts , Melaleuca , Syzygium s.l. and Myrtaceae, using matK 35,36 only . Chronological branch lengths were unavailable for some interpolated taxa regenerate from seed . e Th y recover more slowly than eucalypts 37 and, in these cases, branch lengths were arbitrarily equalized above and below aer ft fire and are forced to accumulate aboveground wood from the interpolated nodes. This did not ae ff ct the inferences of trait evolution in the scratch. When a pine forest planted for carbon capture burns, the eucalypt lineage because the transitions to flammability occurred near the base of trees die and the carbon bank drains. the tree, where branch length information was available. However, branch length uncertainty within Syncarpia, Tristaniopsis and Xanthostemon resulted in wide bounds on the timing estimates of transitions within these lineages (Table 1). Methods Phylogenetics. A dated molecular phylogeny of Myrtaceae was constructed using 66 species with known epicormic anatomy (Supplementary Table S1) and 97 Epicormic anatomy. We scored a matrix for five epicormic structural types 8–11,50 additional taxa, totalling 163 terminals representing higher taxa across the family, across 66 myrtaceous taxa studied to date and for their biome of occurrence on the basis of a recent phylogenetic classification of the family . Most deep-level (Supplementary Table S1). In the first (type A), the bud-forming cells comprise phylogenetic diversity in the family is found within Australia (for example, 14 of meristem strips (that is, radially oriented strips of cells of meristematic appear- 15 tribes in subfamily Myrtoideae), but we also sampled extra-Australian members ance) and are present at all depths in the bark, and in most cases probably extend a of these (where applicable) and the sixteenth tribe (Metrosidereae) to ensure short distance into the outer secondary xylem. For the available bark thickness, this nATuRE CommunICATIons | 2:193 | DoI: 10.1038/ncomms1191 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. nATuRE CommunICATIons | DoI: 10.1038/ncomms1191 ARTICLE structure provides the maximum heat protection for the bud-forming cells. In the 9. Burrows, G. E. Syncarpia and Tristaniopsis (Myrtaceae) possess specialised fire- second type (B), the epicormic buds or bud-forming meristems are located close resistant epicormic structures. Aust. J. Bot. 56, 254–264 (2008). to the cambial surface and covered by numerous layers of dead bark (paperbarks). 10. Waters, D. A., Burrows, G. E. & Harper, J. D. I. Eucalyptus regnans (Myrtaceae): e p Th apery structure provides maximum heat protection for the bud-forming a fire-sensitive eucalypt with a resprouter epicormic structure. Am. J. Bot. 97, cells, but buds need to emerge through numerous bark layers. In the third type (C), 545–556 (2010). epicormic buds are located at the base of a narrow depression in the bark and are 11. Burrows, G. E. et al. A wide diversity of epicormic structures is present in thus about halfway between the bark surface and the cambial surface. This provides Myrtaceae species in the northern Australian savanna biome—implications for an intermediate level of protection for the available bark thickness. In the fourth adaptation to fire. Aust. J. Bot. 58, 493–507 (2010). type (D), epicormic buds are situated at or near the bark surface, giving minimal 12. Fink, S. The occurrence of adventitious and preventitious buds within the bark protection from the heat of a fire. In the fifth type (E), epicormic bud-forming of some temperate and tropical trees. Am. J. Bot. 70, 532–542 (1983). structures are apparently absent. Various processes have been implicated in the 13. Orians, G. H. & Milewski, A. V. 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A likelihood approach to estimating phylogeny from discrete eucalypts originated at the Cretaceous–Palaeogene boundary. Nat. Commun. 2:193 morphological character data. Syst. Biol. 50, 913–925 (2001). doi: 10.1038/ncomms1191 (2011). nATuRE CommunICATIons | 2:193 | DoI: 10.1038/ncomms1191 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved.

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Published: Feb 15, 2011

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