Abstract
Fire has shaped the evolution of many plant traits in fire-prone environments: fire-resistant tissues with heat-insulated meristems, post-fire resprouting or fire-killed but regenerating from stored seeds, fire-stimulated flowering, release of on-plant-stored seeds, and germination of soil-stored seeds. Flowering, seed release and germination fit into three categories of response to intensifying fire: fire not required, weakly fire-adapted or strongly fire-adapted. Resprouting also has three categories but survival is always reduced by increasing fire intensity. We collated 286 records for 20 angiosperm and two gymnosperm families and 50 trait assignments to dated phylogenies. We placed these into three fire-adapted trait types: those associated with the origin of their clade and the onset of fire-proneness [primary diversification, contributing 20% of speciation events over the last 120 million years (My)], those originating much later coincident with a change in the fire regime (secondary diversification, 30%), and those conserved in the daughter lineage as already adapted to the fire regime (stabilisation, 50%). All four fire-response types could be traced to >100 My ago (Mya) with pyrogenic flowering slightly younger because of its dependence on resprouting. There was no evidence that resprouting was always an older trait than either seed storage or non-sprouting throughout this period, with either/both ancestral or derived in different clades and times. Fire-adapted traits evolved slowly in the Cretaceous, 120-65 Mya, and rapidly but fitfully in the Cenozoic, 65-0 Mya, peaking over the last 20 My. The four trait-types climaxed at different times, with the peak in resprouter speciation over the last 5 My attributable to fluctuating growing conditions and increasing savanna grasslands unsuitable for non-sprouters. All experienced a trough in the 40-30-Mya period following a reduction in world temperatures and oxygen levels and expected reduced fire activity. Thick bark and serotiny arose in the Mid-Cretaceous among extant Pinaceae. Heat-stimulated germination of hard seeds is ancestral in the 103-My-old Fabales. Smoke-(karrikin)-stimulated germination of non-hard seeds is even older, and includes the 101-My-old Restionaceae-Anarthriaceae. A smoke/karrikin response is detectable in some fire-free lineages that prove to have a fire-prone ancestry. Among clades that are predominantly fire-prone, absence of fire-related traits is the advanced condition, associated either with increased fire frequency (loss of serotiny and soil storage), or migration to fire-free habitats (loss of thick bark, pyrogenic flowering, serotiny or soil storage). Protea (Africa) and Hakea (Australia) illustrate the importance of stabilisation processes between resprouting/non-sprouting in accounting for speciation events over the last 20 My and highlight the frequent interchange possible between these two traits. Apart from Pinus, most ancestral trait reconstruction relative to fire has been conducted on predominantly Southern Hemisphere clades and this needs to be redressed. Despite these limitations, it is clear that fire has had a profound effect on fire-related trait evolution worldwide, and set the platform for subsequent evolution of many non-fire-related traits. Genetics of the triggering mechanisms remain poorly understood, except the karrikin system for smoke-stimulated germination. We exhort biologists to include fire-proneness and fire-related traits in their thinking on possible factors controlling the evolution of plants.
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Claims 18
Claim · model-written summary
Primary fire-adapted diversification contributed 20% of speciation events over 120 million years.
Not reportedTaxon
Verbatim
e0“primary diversification, contributing 20% of speciation events over the last 120 million years (My)”
Claim · model-written summary
Secondary diversification accounted for 30% of fire-adapted trait assignments.
Not reportedTaxon
Verbatim
e0“secondary diversification, 30%”
Claim · model-written summary
Stabilisation accounted for 50% of fire-adapted trait assignments.
Not reportedTaxon
Verbatim
e0“stabilisation, 50%”
Claim · model-written summary
All four fire-response types trace back more than 100 million years.
Not reportedTaxon
Verbatim
e0“All four fire-response types could be traced to >100 My ago (Mya)”
Claim · model-written summary
Pyrogenic flowering was slightly younger than other fire-response types.
- Outcome
- pyrogenic floweringe0
- Direction
- slightly youngere0
- Qualifier
- because of its dependence on resproutinge0
Not reportedTaxon
Verbatim
e0“pyrogenic flowering slightly younger because of its dependence on resprouting”
Claim · model-written summary
Resprouting was not consistently ancestral to seed storage or non-sprouting.
Not reportedTaxon
Verbatim
e0“There was no evidence that resprouting was always an older trait than either seed storage or non-sprouting throughout this period”
Claim · model-written summary
Fire-adapted traits evolved slowly in the Cretaceous and rapidly but intermittently in the Cenozoic.
Not reportedTaxon
Verbatim
e0“Fire-adapted traits evolved slowly in the Cretaceous, 120-65 Mya, and rapidly but fitfully in the Cenozoic, 65-0 Mya, peaking over the last 20 My.”
Claim · model-written summary
Resprouter speciation peaked in the past five million years.
Not reportedTaxon
Verbatim
e0“the peak in resprouter speciation over the last 5 My”
Claim · model-written summary
All four fire-response trait types had a trough 40–30 million years ago.
Not reportedTaxon
Verbatim
e0“All experienced a trough in the 40-30-Mya period”
Claim · model-written summary
Thick bark and serotiny originated among extant Pinaceae in the Mid-Cretaceous.
Verbatim
e0“Thick bark and serotiny arose in the Mid-Cretaceous among extant Pinaceae.”
Claim · model-written summary
Heat-stimulated hard-seed germination was ancestral in Fabales.
Verbatim
e0“Heat-stimulated germination of hard seeds is ancestral in the 103-My-old Fabales.”
Claim · model-written summary
Smoke-stimulated non-hard-seed germination was older and included Restionaceae-Anarthriaceae.
Verbatim
e0“Smoke-(karrikin)-stimulated germination of non-hard seeds is even older, and includes the 101-My-old Restionaceae-Anarthriaceae.”
Claim · model-written summary
Some fire-free lineages retain smoke or karrikin responses consistent with fire-prone ancestry.
Verbatim
e0“A smoke/karrikin response is detectable in some fire-free lineages that prove to have a fire-prone ancestry.”
Claim · model-written summary
In fire-prone clades, absence of fire-related traits was inferred to be advanced.
Verbatim
e0“Among clades that are predominantly fire-prone, absence of fire-related traits is the advanced condition”
Claim · model-written summary
Fire-prone clades lost serotiny and soil storage with increasing fire frequency.
Not reportedTaxon
Verbatim
e0“associated either with increased fire frequency (loss of serotiny and soil storage)”
Claim · model-written summary
Migration to fire-free habitats was associated with loss of thick bark, flowering, serotiny or soil storage.
- Outcome
- loss of thick bark, pyrogenic flowering, serotiny or soil storagee0
- Setting
- fire-free habitatse0
Not reportedTaxonDirection
Verbatim
e0“migration to fire-free habitats (loss of thick bark, pyrogenic flowering, serotiny or soil storage)”
Claim · model-written summary
Protea and Hakea showed repeated interchange between resprouting and non-sprouting states.
Organisms pictured · Representative pictures of the matched species, not figures from the paper.


Verbatim
e0“Protea (Africa) and Hakea (Australia) illustrate the importance of stabilisation processes between resprouting/non-sprouting in accounting for speciation events over the last 20 My and highlight the frequent interchange possible between these two traits.”
Claim · model-written summary
Authors recommend incorporating fire-proneness and fire-related traits into studies of plant evolution.
- Taxon
- plantsViridiplantaee0
- Outcome
- include fire-proneness and fire-related traitse0
Verbatim
e0“We exhort biologists to include fire-proneness and fire-related traits in their thinking on possible factors controlling the evolution of plants.”