Paper · 2018 · Biological reviews/Biological reviews of the Cambridge Philosophical Society

Evolutionary history of fire‐stimulated resprouting, flowering, seed release and germination

Byron B. Lamont; Tianhua He; Zhaogui Yan

18
claims
18
verbatim quotes
141
citations
2
research areas
—
Not open access

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

Observationobservedoriginal resultmeasured

Claim · model-written summary

Primary fire-adapted diversification contributed 20% of speciation events over 120 million years.

Outcome
speciation eventse0
Value
20%e0
Qualifier
over the last 120 million years (My)e0

Not reportedTaxon

Verbatim

e0

“primary diversification, contributing 20% of speciation events over the last 120 million years (My)”

✓ located verbatim in the source · abstract, characters 820–919 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Secondary diversification accounted for 30% of fire-adapted trait assignments.

Outcome
secondary diversificatione0
Value
30%e0

Not reportedTaxon

Verbatim

e0

“secondary diversification, 30%”

✓ located verbatim in the source · abstract, characters 996–1026 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Stabilisation accounted for 50% of fire-adapted trait assignments.

Outcome
stabilisatione0
Value
50%e0

Not reportedTaxon

Verbatim

e0

“stabilisation, 50%”

✓ located verbatim in the source · abstract, characters 1112–1130 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

All four fire-response types trace back more than 100 million years.

Outcome
fire-response typese0
Value
>100 My ago (Mya)e0

Not reportedTaxon

Verbatim

e0

“All four fire-response types could be traced to >100 My ago (Mya)”

✓ located verbatim in the source · abstract, characters 1133–1198 · show in text ↑
Observationobservedoriginal resultmeasured

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”

✓ located verbatim in the source · abstract, characters 1204–1281 · show in text ↑
Observationobservedoriginal resultno effectmeasured

Claim · model-written summary

Resprouting was not consistently ancestral to seed storage or non-sprouting.

Outcome
resproutinge0
Direction
no evidencee0
Comparator
seed storage or non-sproutinge0

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”

✓ located verbatim in the source · abstract, characters 1283–1412 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Fire-adapted traits evolved slowly in the Cretaceous and rapidly but intermittently in the Cenozoic.

Outcome
Fire-adapted traitse0
Direction
rapidly but fitfullye0
Qualifier
peaking over the last 20 Mye0

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.”

✓ located verbatim in the source · abstract, characters 1483–1629 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Resprouter speciation peaked in the past five million years.

Outcome
resprouter speciatione0
Direction
peake0
Value
5 Mye0

Not reportedTaxon

Verbatim

e0

“the peak in resprouter speciation over the last 5 My”

✓ located verbatim in the source · abstract, characters 1685–1737 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

All four fire-response trait types had a trough 40–30 million years ago.

Outcome
troughe0
Value
40-30-Myae0

Not reportedTaxon

Verbatim

e0

“All experienced a trough in the 40-30-Mya period”

✓ located verbatim in the source · abstract, characters 1849–1897 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Thick bark and serotiny originated among extant Pinaceae in the Mid-Cretaceous.

Taxon
PinaceaePinaceaee0
Outcome
Thick bark and serotinye0
Qualifier
Mid-Cretaceouse0

Verbatim

e0

“Thick bark and serotiny arose in the Mid-Cretaceous among extant Pinaceae.”

✓ located verbatim in the source · abstract, characters 1996–2070 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Heat-stimulated hard-seed germination was ancestral in Fabales.

Taxon
FabalesFabalese0
Outcome
Heat-stimulated germination of hard seedse0
Qualifier
103-My-olde0

Verbatim

e0

“Heat-stimulated germination of hard seeds is ancestral in the 103-My-old Fabales.”

✓ located verbatim in the source · abstract, characters 2071–2152 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Smoke-stimulated non-hard-seed germination was older and included Restionaceae-Anarthriaceae.

Taxon
Restionaceae-Anarthriaceaee0
Outcome
Smoke-(karrikin)-stimulated germination of non-hard seedse0
Direction
even oldere0
Qualifier
101-My-olde0

Verbatim

e0

“Smoke-(karrikin)-stimulated germination of non-hard seeds is even older, and includes the 101-My-old Restionaceae-Anarthriaceae.”

✓ located verbatim in the source · abstract, characters 2153–2281 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Some fire-free lineages retain smoke or karrikin responses consistent with fire-prone ancestry.

Taxon
fire-free lineagese0
Outcome
smoke/karrikin responsee0
Qualifier
fire-prone ancestrye0

Verbatim

e0

“A smoke/karrikin response is detectable in some fire-free lineages that prove to have a fire-prone ancestry.”

✓ located verbatim in the source · abstract, characters 2282–2390 · show in text ↑
Observationauthor interpretationoriginal resultmeasured

Claim · model-written summary

In fire-prone clades, absence of fire-related traits was inferred to be advanced.

Taxon
clades that are predominantly fire-pronee0
Outcome
absence of fire-related traitse0
Qualifier
advanced conditione0

Verbatim

e0

“Among clades that are predominantly fire-prone, absence of fire-related traits is the advanced condition”

✓ located verbatim in the source · abstract, characters 2391–2495 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

Fire-prone clades lost serotiny and soil storage with increasing fire frequency.

Outcome
loss of serotiny and soil storagee0
Direction
associatede0
Setting
increased fire frequencye0

Not reportedTaxon

Verbatim

e0

“associated either with increased fire frequency (loss of serotiny and soil storage)”

✓ located verbatim in the source · abstract, characters 2497–2580 · show in text ↑
Associationobservedoriginal resultmeasured

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)”

✓ located verbatim in the source · abstract, characters 2585–2684 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Protea and Hakea showed repeated interchange between resprouting and non-sprouting states.

Taxon
Protea (Africa) and Hakea (Australia)ProteaHakeae0
Outcome
resprouting/non-sproutinge0
Direction
frequent interchangee0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Protea
Protea · Taxon · picture of the genus (one of its species)Chinasaur at English Wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗
Hakea
Hakea · Taxon · picture of the genus (one of its species)JJ Harrison ( https://www.jjharrison.com.au/ ) · CC BY-SA 3.0 · Wikimedia Commons ↗

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.”

✓ located verbatim in the source · abstract, characters 2686–2940 · show in text ↑
Recommendationauthor interpretationoriginal resultbasis n/a

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.”

✓ located verbatim in the source · abstract, characters 3429–3574 · show in text ↑