Ancient DNA and UV-B
radiation and its ecological
and evolutionary impacts
John Birks
Bio 301 Lecture 4
Introduction
Explanation of distributional patterns
Palaeobiological data
Genetic data
Integration of palaeobiology and phylogeography
‘First’ and ‘second’ generation studies
‘Third’ and ‘fourth’ generation studies
Ancient DNA (a-DNA)
Human a-DNA
Analytical criteria
‘Spectacular’ a-DNA studies
Ancient plant DNA
Conclusions
UV-B radiation – A driver of speciation?
Introduction
Late-Permian extinction event
Species ‘swarms’
Biological responses to changing UV-B over
time
UV-B, diversity, and speciation
Why is pollen yellow?
Why are there so many species in the tropical
rain forest?
Conclusions
INTRODUCTION
Explanation of Distributional Patterns
Geographical distribution of a species derives from
• Contemporary processes (ecophysiological
processes, species interactions, disturbance
regimes, dispersal and establishment, etc.)
• Historical processes (decadal to centennial-scale
legacies of disturbance or dominance in local
patches or areas to deeply rooted phylogenetic
divergences at continental to global scales)
Quaternary environmental changes over the past
2.6 million yrs of Earth’s history have had
dramatic biogeographical and ecological
effects but not so dramatic evolutionary impacts.
Signatures of Quaternary history are apparent in
the spatial patterns of species distributions and
genetic variation across the globe today.
Species have adjusted their geographical ranges in
response to environmental (mainly climate)
change during the Quaternary – strong
individualistic responses, migrations and
habitat shifts, but few extinctions.
These historical events leave clues of two kinds
on the landscape
• Physical remains of ancient organisms
preserved in a few local geological settings,
providing direct fossil evidence of their former
existence “the factual basis for phytogeography”
• Genetic composition as inferred from
phenotypic traits and molecular markers
Both types of clues were used since the mid 19th
century to infer the biogeographical history of
species – Charles Darwin, Charles Lyell, Asa Gray,
Alfred Russell Wallace
Keenly gathered information from modern-day
distributions and morphological variation and from
Quaternary (and Tertiary) fossils to support their
arguments and discussions (cf. Lyell and Darwin)
The use of these dual sources were greatly refined
in the late 19th and 20th centuries
Plant macrofossils – Clement and Eleanor Reid,
Alfred Gabriel Nathhorst, Knud Jensen, Frank
Mitchell, Harry Godwin, Bill Watts, Hilary Birks, and
others
Modern distributional patterns, phenotypic
traits, and co-occurrence patterns – Axel Blytt,
Eric Hultén, Rolf Nordhagen, Eilif Dahl, Donald
Pigott, Max Walters, and others
Since 1960s, major developments in both
approaches
• Quaternary palaeobiology – 14C-dating, synthesis
of pollen and macrofossil data into continentalscale data-bases allowing synoptic mapping of
distributional patterns through time (e.g. isochrone
and isopollen maps to study migration patterns)
• Biogeographical evidence – developed from species
occurrences to morphological and phenotypic traits
to biochemical markers to, most recently,
molecular DNA markers.
Despite these developments, surprisingly few
attempts to integrate the wealth of genetic and
palaeobiological data now available to elucidate
biogeographical history.
Notable exceptions
Fagus sylvatica Magri et al. (2006) New Phytol.
171: 199-221 (see Lecture 2)
Quercus robur & Q. petraea
Petit et al. (2002) Forest Ecol
Management 156: 49-74
Also Pinus and Abies in Europe
See Petit et al. (2008) Science 330: 1450-1452
Palaeobiological Data
All historical sciences have to rely on imperfect and
fragmentary evidence
Palaeobiological evidence of ecological history restricted to a
limited number of depositional situations (lack of oxygen,
permanently waterlogged, etc.). Such situations are absent from
many regions and are unevenly distributed elsewhere.
Site density decreases and age uncertainties increase with age.
Pollen data provide complex view of past vegetation, distorted
by differential pollen production and dispersal and by taxonomic
smoothing (nearly all grass pollen is one pollen type). A Fagus
(beech) pollen grain in lake sediments may have come from a
tree growing on the lake shore or from a population 1, 10, or
100 km away. No way of knowing!
Macrofossil data impart taxonomic and spatial precision but
they are idiosyncratic in relation to sampling, occurrence, and
representation. Some lakes are ‘good’ for macrofossils, others
are ‘very poor’ for no obvious reasons
Despite its limitations, the palaeobiological record
does tell us something about past species
distributions and the mechanisms behind their
dynamics.
1. Pollen and macrofossils can be used together to
refine interpretations of each other
2. Spatial-scale differences between pollen and
macrofossils can reveal patterns across a range of
scales when data are mapped in geographical
networks
However, both pollen and macrofossil data are blind to
several features of plant migration
1. Even with dense network of sites, cannot exclude
possibility that some isolated population was too small or
too far away from the site to be detected. Incomplete
picture, particularly of small, isolated populations.
2. Tells us nothing about dynamics below morphological
species level. What were the source populations for
colonisation at a particular site? What were the spatial
and temporal patterns of range expansion?
1) expanding front, 2) series of jump dispersals with secondary
coalescence, 3) set of parallel pathways from multiple sources, 4)
pincer movement from two directions, 5) sequence of successive
waves representing different genotypes, 6) some combination of these
Palaeobiological data often show patterns corresponding
to one or more of these hypotheses (e.g. 1,2,4) but
spatial and temporal limitations preclude definitive
interpretations.
Genetic Data
Genetic data contain information below the species level
that can help to address these and related questions (e.g.
Fagus sylvatica study of Magri et al. 2006).
But the genetic evidence has its own limitations.
1. Can only obtain evidence where extant native
populations occur today
2. Such populations and their associated genetic patterns,
represent the culmination of a long and presumably
complex history with erasures, overlays, and other
distortions in their DNA
3. The spatial genetic patterns themselves make little
sense except in the context of the history of the
populations. Interpretation governed by i) density of
sampling, ii) number and quality of genetic markers,
and iii) accuracy and sophistication of the
palaeobiological data and insights into the genetic data
Integration of Palaeobiology and
Phylogeography
Both palaeobiological and genetic data are needed
together to understand distributional patterns
Have tended to develop along separate pathways with,
until recently, an important asymmetry
1. Palaeobiologists have, with few exceptions, relied
exclusively on fossil records as their source of
inference and have ignored (or even questioned) the
relevance of genetic evidence.
2. Phylogeographers have recognised from the outset
that interpretation of genetic patterns requires
independent knowledge of history, and have used
(not always correctly!) geological, palaeoclimatic,
and palaeoecological literature to generate and test
hypotheses to explain observed genetic patterns
First- and Second-Generation Studies
With few exceptions, phylogeographers did not enlist the
help of palaeobiologists with the result that many firstgeneration phylogeographic interpretations were based
on overly simplistic views of Quaternary biogeography
and climatic history. They miss the richness and
complexity of Quaternary climate and vegetation
dynamics revealed by recent detailed palaeoecological
studies at a range of spatial and temporal scales
completed in the last two decades.
When DNA-based phylogeography was getting underway,
understanding of Quaternary dynamics was undergoing
rapid change and thus phylogeographers were using
Quaternary literature and data-bases that were fast
becoming obsolete. No excuse for repeating the mistakes
of 1987 25 years later in 2012!
Recommend reading
Magri et al. (2006) New Phytologist 171: 199-221
(Fagus)
Petit et al. (2002) Forest Ecology and Management
156: 49-74 (Quercus)
Both exemplary studies involve DNA studies of large
numbers of extant populations throughout the
geographical range of the tree, make full use of
palaeobiological data, and careful data analysis
where ‘the data are allowed to speak for themselves’
These represent state-of-the-art second-generation
studies integrating Quaternary palaeobiology and
phylogeography
What about future third or even fourth generation
studies?
Third- and Fourth-Generation Studies
Third generation – not only incorporate sampling of
new genetic data and use all palaeobiological data,
but also include targetted palaeobiological
sampling to obtain new and/or better
palaeobiological records. Productive strategy can
develop in which genetic studies tell palaeobiologists
where data are critically needed and palaeobiological
studies can identify targets for intensive genetic
sampling. Need continuous dialogue between
phylogeographers and palaeobiologists.
Fourth generation – integrated palaeobiological
and phylogeographical studies may lead to the
fourth-generation fusion of physical and genetic
evidence via ancient DNA (a-DNA) studies.
Development of spatial arrays of a-DNA records
integrated with modern phylogeography, standard
but detailed palaeobiological studies, and
independent palaeoclimatic records (e.g. stable
isotopes, chironomid-inferred temperatures)
could, in theory, revolutionise our understanding
of what actually happens to species and
populations in changing environments.
What is the status of a-DNA studies?
ANCIENT DNA (a-DNA)
Ancient DNA – any DNA recovered from biological
samples can provide a direct approach to
reconstructing history of life
• Bones and scales
• Preserved seeds and resting eggs
• Permafrost and ice samples
• Fossil animals
• Fossil plant material (seeds, pollen)
• Sediments
a-DNA may provide insights into extant and extinct
populations and species and inform us about
biological change through time
In theory, could provide ‘evolutionary time
travel’ to explore empirically how biota and
species, including Homo sapiens, have
responded to environmental change. Results are
of importance to biologists, ecologists,
phylogeographers, anthropologists, medical
scientists, geneticists, climatologists, and
archaeologists and economists interested in the
economies of past civilisations.
a-DNA was, in 2010, considered one of the top
ten ‘big ideas’ of the decade, leading to
• draft nuclear sequence of Neanderthals
• discovery of a new hominid from Denisova
Cave in Siberia
Human a-DNA
Gibbons (2010)
Calloway (2011)
Gibbons (2011)
modern genomes 
Neanderthal remains 
Arrows show commonly
accepted migration
routes of modern
humans out of Africa
African
populations
genetically
highly diverse
Bustamante & Henn (2010)
Denisova Cave  third
group with distinct
ancient genome
a-DNA suggests two episodes of limited gene flow
1) genetic mixing from Neanderthals to modern humans shortly
after exit from Africa
2) subsequent mixing with the Denisovan population. Only
affected ancestors of present-day Melenasians who colonised
Papua New Guinea ~45,000 years ago.
a-DNA is a major research field in archaeology
2001
2005
Such great enthusiasm for a-DNA was not always
the case
• a-DNA molecules from recent material are
characteristically degraded into short pieces
and present only in trace amounts
• contamination and the synthesis of spurious
DNA sequences via PCR (polymerase chain
reaction) are major risks
• early claims in 1980s of 80 million year old
dinosaur DNA turned out to be human DNA
• frequent bacterial or human contamination of
proposed a-DNA samples has resulted in many
flawed studies
Analytical Quality Criteria
a-DNA labs now have nine criteria for authenticity
as standardised criteria. Still not always possible to
follow them all. In practice, many a-DNA studies
incorporate only a subset of the nine criteria even
now.
Criteria (Cooper & Poinar 2000)
• Physically isolated work area
• Control amplifications – multiple extractions and PCR
controls
• Appropriate molecular behaviour – amplification
strength carefully selected
• Reproducibility
• Cloning – verify PCR sequences by cloning amplified
products
• Independent replication by different labs
• Biochemical preservation – evidence for quality of
preservation
• Quantitation – competitive PCR
• Associated remains – examine associated material
Ancient DNA:
‘Do it right or not at all’ – Cooper & Poinar (2000)
See papers available from the Student Portal by
de Bruyn et al. (2011)
Gilbert et al. (2005)
Hebsgaard et al. (2005)
on assessing a-DNA studies
Other spectacular a-DNA studies that pass at least 6
of the 9 criteria (Papers on Portal – discussion in Class 6)
Woolly
mammoths
Debruyne et al. (2008) Poinar et al. (2006)
Gibbons (2005, 2010) Miller et al. (2008)
Pennisi (2005)
Cave bears
Knapp et al. (2009)
Noonan et al. (2005)
PalaeoEskimo
Dalton (2010)
Curry (2007)
Rasmussen et al. (2008)
Lambert & Huynen (2010)
Reindeer
hunting/
husbandry
Ice-core
study
Bjørnstad et al. (2012)
Willerslev et al. (2007)
Ancient Plant DNA
a-DNA from plants extracted from permafrost soils,
dry cave earths, lake sediments, fossil pollen, fossil
seeds, fossil wood in archaeological sites, peat,
rodent middens
Also bacterial and fungal DNA from lake sediments
and permafrost soils
a-DNA preserved in varying amounts and with varying
preservation in a range of sedimentary environments
– not necessarily of great age
Wood remains
Peat
Bacteria
Leaves
1000 yrs
10-450 yrs
7000 yrs
17-20 million yrs
Liepelt et al. (2006)
Suyama et al. (2008)
Madeja et al. (2009)
Kim et al. (2004)
a-DNA from permafrost soils in Siberia
NE Siberia, cores 2-30 m deep, extracted
chloroplast DNA and animal DNA 30,000-40,000
years old.
Found at least 19 vascular plant taxa Cyperaceae, Poaceae, Liliaceae, Ericaceae,
Salicaceae, Fabaceae, Rosaceae, Polygonaceae,
Caryophyllaceae, Asteraceae, Papaveraceae,
Campanulaceae, etc., plus 3 more families.
Also mammoth, musk ox, horse, lemming, hare,
and bison DNA.
Willerslev et al. (2003) Science 300: 791-795; 407
Change in plant composition and diversity through time in permafrost core samples.
(A) For each time period, the proportion of shrubs, herbs, and mosses observed is
indicated, along with the proportion of all taxa that are detected or not detected in
samples from the previous time point. Clone sequences 96% identical are assumed
to represent one taxon. (B) Changes in taxonomic diversity through time, as
measured by the number of sequence groups (clone sequences with <96%
similarity) divided by the total number of clone sequences obtained for that sample.
To standardise the number of clones sequenced, sequence diversity was measured
in each sample with 1000 data sets of 32 randomly chosen clones. Black dots
represent permafrost samples; white dots represent New Zealand cave samples.
Being used as a ‘fossil’ to identify fossils and to
estimate biodiversity. Not being used as a
palaeogenetic tool.
Permafrost soil contains not only plant a-DNA but
also megafaunal a-DNA (mammoth, bison, horse,
etc.), and a-DNA from fungi, yeasts, lichen
mycobionts, plant-parasitic fungi, even treeassociated macrofungi (?in LGM tundra?).
Megafaunal a-DNA could be from faeces, hair, skin,
and nails.
Large and unknown source area.
Sønstebø et al. (2010) Molecular Ecology Resources
10: 1009-1018
Looked at a-DNA with the P6 loop using ‘nextgeneration sequencing’ in two permafrost soils from
Siberia (15,810 and 22,960 14C yrs BP)
Identified 47 taxa in 22,960 yr BP sample and 17 in
15,810 yr BP sample. Data-base of 842 arctic
species
Results make good sense ecologically, data are
semi-quantitative (%), and agree with detailed plant
macrofossil data. a-DNA used as a palaeobiological
tool not a palaeogenetic tool.
Is a-DNA leaching and movement a factor in soil
DNA studies?
Haile et al. (2007) Molecular Biology & Evolution 24: 982-989
Two cave sites on North Island, New Zealand. Sheep
are an introduced animal so its DNA is a marker of
contamination by modern DNA.
Found sheep DNA in strata that contained moa DNA
(an extinct flightless bird). DNA had migrated
downwards.
Amount of sheep DNA decreased as age of
sediments increased.
Sedimentary a-DNA unlikely to be wind-borne and
physical remains of organisms or their excreta must
be incorporated in the sediments for their DNA to be
detected.
Biogeographical shifts inferred from a-DNA
Kuch et al. (2002) Molecular Ecology 11: 913-914
11,700 yr rodent midden from Atacama Desert,
Chile
a-DNA
5 families, 3 orders
Macrofossils
13 families
More diverse flora than today – more Poaceae,
Solanaceae, and Fabaceae. All found today at
higher elevations and in more humid areas.
a-DNA used to identify the rodent
that formed the midden as
Phyllotis limatus, only found
100 km north of the site today.
Biogeographical shifts inferred from a-DNA
Poinar et al. (1998) Science 281: 402-406
Molecular coproscopy of dung of extinct ground
sloth in Gypsum Cave, Nevada
Plants present occur today at elevations 800 m
higher than the cave.
Major ecological shifts.
Ancient DNA and pollen
So far, the organisms that produced the a-DNA
are not all known and a-DNA is being used as a
means of identification.
Alternative approach is to extract a-DNA from
identified fossils to reconstruct past lineages.
Pollen contains haploid DNA and is the means of
dispersal to haploid DNA of ovules. Consists of
2-3 haploid cells (large vegetative cells including
several plastids and mitochondria). Organelle
DNA is thus present in pollen.
Pollen from species with paternal inheritance of
plastid DNA (e.g. 6 of the 7 families of conifers) is
rich in plastid DNA at maturation, and the
existence of these multiple copies makes this
source of DNA the best prospect for a-DNA studies
using pollen.
Nuclear DNA, in contrast, present only as a single
copy (and is subject to recombination that
complicates its use in phylogeography).
Plant mitochondrial DNA evolves too slowly,
whereas plastid DNA appears to be ideal for
phylogeographical reconstruction.
As a source of a-DNA, pollen has a disadvantage in
that from each grain there is only one change for
extracting DNA of each type (nuclear, plastid,
mitochondrial) in contrast to bone, tissue, or
wood. Replicability comes from the ready access to
a large number of pollen grains (e.g. 100-1000),
giving the possibility of a statistical population of
genotypes, rather than a strong dependence on
the successful extraction from a few (or even one)
genotypes.
Methods: Bennett & Parducci (2006) The Holocene
16: 1031-1034
Applications
Parducci
et al. (2005)
Chloroplast DNA from Pinus pollen in central
Sweden 100 and 10,000 yrs old. Identical –
no change
Suyama
et al. (1996)
Chloroplast DNA from Abies pollen >100,000
yrs old in Japan
Paffetti
et al. (2007)
Chloroplast DNA from Fagus orientalis pollen
(angiosperm) 45,000 yrs old
Magyari
et al. (2011)
Chloroplast DNA from Picea pollen and cones
from South Carpathians. Showed a-DNA from
early Holocene similar to today but earlier
forms had a greater level of genetic
variation. Loss of ancient allele types probably
due to repeated bottlenecks during the
Holocene. Major discovery – loss of genetic
diversity during Holocene.
Magyari et al. (2011)
Pollen a-DNA future directions
Pollen is probably the most abundant lateQuaternary fossil. Potentially ideal in a-DNA studies
1. Investigate population-level dynamics in time and
space
2. Trace ancestry of populations and develop
phylogenetic trees that include extinct taxa
3. Develop technique over the last glacial-interglacial
cycle, and investigate the extent to which
evolutionary changes are influenced by climatic
changes of a glacial-interglacial oscillation.
Much to be done. Very demanding work. Results so
far not particularly exciting but things may hot up
soon!
a-DNA from macrofossils in lake sediments
Anderson-Carpenter et al. (2011) BMC Evolutionary Biology 11: 30
Looked at a-DNA in bulk sediment and in macrofossils
from 4 tree species in 7 small lakes in Upper Michigan
and Wisconsin
sen = senescent material
Could only extract
DNA from
sediments younger
than 4600 yrs old.
Regional-scale
feature, possibly
due to drop in lakelevels before 4000
yrs ago, leading to
better oxygenated
conditions and
decay
a-DNA and genetic responses to environmental
change
Surprisingly few such studies!
Epp et al. (2010) J. Paleolimnol. 43: 939-954
Alkaline-saline crater lake in Kenya.
Examined a-DNA of Brachionus rotifers
Dominated by B (red), then a
change to A (blue) after
deposition of volcanic ash,
changing back to B but with a
new haplotype D (green) while
lake levels were falling. Subtle
genetic shifts.
Hadly et al. (2004) PLoS Biology 2: e290
Two small mammal species Microtus
montanus and Thomomys talpoides in
Lamar Cave, Wyoming during lateHolocene climatic change. Used a-DNA
to compare two independent estimates
of population size (ecological and
genetic).
Showed that population size decreased when
climate changed and one species showed declining
genetic diversity, as predicted from simple
population genetic models. Consistent with
selection hypothesis, but independent evidence
suggests differences in gene flow which depends on
the life-history strategy of the species.
Hofreiter et al. (2012) Quat. Sci. Rev. 33: 1-13
DNA recovery through time for coprolites (human, sloth) and
sediments (permafrost, temperate, marine, and freshwater).
Extends to 500,000 yrs, mainly last 10,000 yrs
Conclusions
a-DNA studies are, with considerable care, possible
Need very great care in sampling, laboratory
techniques, and analytical techniques
Need to follow the 9 criteria of Cooper & Poinar (2000)
– not always done
In Quaternary palaeobiology, a-DNA has been
primarily used as a means of identifying fossil taxa.
Very little done on genetic variability, adaptation, or
environmental impacts
Great contributions in archaeology
Botanical applications perhaps a touch of ‘much ado
about nothing’. Will no doubt change in the future
UV-B RADIATION – A DRIVER OF
SPECIATION?
UV-B radiation (280-315 nm)
currently 1.5% of incoming solar
radiation. Amount changes over time
Influences stratosphere
and troposphere and
hence solar radiation,
atmospheric circulation,
precipitation, and
temperature near Earth’s
surface.
Can, in conjunction with
solar wind and solar
cosmic rays, cause small
variations in solar activity
that can be amplified to
causes significant
climatic changes.
Why should UV-B be potentially important
in speciation?
Willis et al. (2009) J. Biogeography 36: 1630-1644
Wavelength: 280-315 nm
Common effects of 20% elevated UV-B are
• reduced plant height
• decreased shoot mass
• reduced leaf area
• increased UV-B absorbing pigments
• increased genetic mutations
Elevated UV-B levels have been shown to change the
rate of mutation and hence genetic change and
speciation rates.
Much work has been done on effects of elevated
UV-B on organisms and ecosystems, including
human health
Individuals
Reduction in plant height and above-ground
biomass
Decreased shoot mass
Reduction in leaf area
Increase in UV-B absorbing pigments in
cuticles, pollen and spores, wood, and
seed coats
Genetic mutations
Decrease in overall fitness
Ecosystems
Changes in nutrient cycling
Decreased shoot mass
Increased rates of N fixation
Increased litter decomposition
2001
2009
UV-B radiation currently 1.5% of incoming solar
radiation
Major changes have occurred in recent times and
in Deep-Time
In some time intervals, areas have received 6080% more UV-B than today
Possible mechanisms
Changes in thickness of stratospheric ozone layer
Solar activity
Milankovitch orbital fluctuations
Volcanic events
Variations in cloud cover
Late Permian Mass Extinction Event
(250 Myr ago)
Most devastating ecological event of all time, made
worse by two earlier events at 260 and 270 Myr.
Ecosystems were destroyed worldwide
50% of all families of marine and terrestrial
animals went extinct
80-96% species loss
Probably only 4-20% species survived
Total extinction of blastoid echinoderms,
tabulate and rugose corals, graptolites, and
trilobites. Two thirds of tetrapod families
went extinct
Biologically a few taxa appeared in almost all areas
and there seems to have been a quick taxonomic
recovery.
When examined in fine stratigraphical detail,
diversity never recovered to pre-extinction levels.
Sahney &
Benton (2008)
What may have caused this massive mass extinction?
No evidence for asteroid impact.
Current hypothesis centres on the Siberian Traps, 2
million km3 of basalt lava covering 1.6 million km2 of
Eastern Russia at depths of 400-3000 m.
Massive eruption in less than 1 Myr right at the end of
the Permian.
Major changes in oxygen isotopes at end of Permian
suggesting a global temperature rise of 6°C. This could
reduce ocean circulation and cause a lack of oxygen
(anoxia) on sea-floor.
But carbon isotopes show a sharp negative change from
2-4 parts per thousand to -2 parts per thousand. This
implies a dramatic increase in the light 12C isotope. But
what caused this?
Gas hydrates – formed from remains of marine
plankton that sink to sea-bed and become buried.
Over millions of years, huge amounts of carbon
are transported to deep oceans and are trapped
as methane in a frozen ice lattice.
If gas hydrates are disturbed by an earthquake or
sea-water warms, gas hydrates may be dislodged
and methane is released and rushes to surface.
Gas hydrates are at depth and under high
pressure. In rush to surface, gas hydrates expand
as much as 160 times. Contain carbon as the light
12C isotope.
Current idea – largely driven by the rise of
atmospheric CO2 and global warming
Siberian Trap volcanism
 CO2
 CO2
 SO4- and NO3-
 CH4
Global warming
Acid rain
Terrestrial
extinctions
Melting of
gas hydrates
 ocean
circulation
Marine anoxia
 upwelling
 productivity
Marine extinctions
What effects did mass extinction events have on plants?
Originally thought that there was little or no evidence for
mass extinction in the plant fossil record.
Is this likely?
If you go to a zoo and shoot all the animals, you have the end
of the zoo.
If you go to a plant nature reserve and burn all the plants,
within 2-10 years, a large number of species reappear.
Also in Gould’s scheme of evolutionary processes, without
mass extinctions, dinosaurs would still dominate the
vertebrate world. If there are no mass extinctions in the plant
world, modern vegetation would be dominated by lycopods,
Bennettitales, or early gymnosperms like cycads.
Do we need an upper layer in Gould’s scheme for plant
evolution – one driven by competition and selection of
lineages? A return to Darwinian principles of natural selection
but at the level of species rather than individuals as in natural
selection.
McElwain & Punyasena (2007) TREE 22: 548-557
Plants and mass extinction events
Event
Fauna family (%)
Flora family (%)
Terrestrial
Marine
Global
Regional
?
24
?
?
Late Devonian
44
28
<5
30-40
Late Permian
62
50
<5
19
Late Triassic
22
23
<5
17
6
15
<5
18-30
Late Ordovician
Late Cretaceous
Floral extinctions much less than animal extinctions
at global scale, but more extensive at the regional
scale.
Now appears that although plants persisted across
mass extinction boundaries, there may have been
major changes in their abundance.
Consider Late Permian mass extinction event –
C isotope shift
CO2 (ppmv)
Asteroid impact
Volcanism
Global temp change (°C)
Late Permian
–3-5%
>2000 
(+)
++ (Siberian Traps)
>8
Change in plant
community
structure and
d13C isotope
shifts (red line).
Major animal
extinction times
shown in grey.
McElwain &
Punyasena (2007)
Late Permian – many malformed lycopod spores, possibly a
result of increased UV-B radiation.
See plant community instability soon after mass extinctions,
rather than global plant extinctions. Plant community changes
may have had effects on terrestrial ecosystem functioning such
as biogeochemical cycles.
Severe disruption of
stratosphere ozone
balance (80% thinning)
during massive Siberian
Trap volcanic eruptions –
may have increased UV
radiation and caused
widespread mutation.
Abundant mutant
deformed Lycopodium
spores and pollen grains
at this time on several
continents.
Foster & Afonin (2005)
Visscher et al. (2004)
Altered plant genomes and their proper functioning,
and caused dieback of vegetation, especially woody
plants.
“Mutation caused by cosmic radiation could account
for not only extinction, but also for accelerated
origination of clades”
Schindewolf (1954)
Common patterns of plant changes at mass
extinction events
1. Permanent or temporary loss of ecological dominants
at regional scales over thousands to millions of years.
2. Recoveries over millions of years.
3. Prolonged instability at Late Triassic and Late Permian
events.
4. Although few plant families were lost, extinction at
species level was highly selective. High loss of insectpollinated taxa at Late Cretaceous event and of insectpollinated cycads at the Late Triassic event.
5. Most post extinction-event survivors had low
abundances before the event. Probably poor
competitors in pre-event time, but competitive
balances changed after extinction event.
6. Likelihood of extinction changed. Rarities as
defined as having low relative abundances in last
quartile (25%) of rank distributions went extinct
more at Late Triassic event but not at the other
events.
7. Plant families show incredible resilience across
the mass extinction events. Do not show mass
extinctions but show major ecological changes
with impacts on ecosystem function – primary
productivity and run-off rates and biogeochemical
cycles (e.g. increased particulate and nutrient flux
from land into oceans at Late Permian and Late
Devonian).
8. No primary role in the overall patterns of plant
evolution, in contrast to animals.
9. Plant groups show amazing taxonomic resilience
across faunal mass extinction events, possibly to
the great breadth of morphological, anatomical,
and physiological traits that plants have. Great
survivors!
10.Can we learn anything from the mass extinction
events concerning the present sixth mass
extinction in Earth’s history?
• reproductively specialised groups suffered
disproportionately in previous mass extinctions,
providing Deep-Time support for predictions
from metapopulation dynamics
• need to consider assemblages as a whole rather
than individual species in modelling future
responses
Three levels of processes controlling
evolutionary patterns as seen in the
geological record – Gould (1985)
Level
Period
Cause
Evolutionary processes
First
-
-
Microevolutionary
change through natural
selection in more-or-less
stable assemblages
Second -
Geographic
isolation
(continental
drift, creation
of islands, etc)
Macroevolutionary
change through
speciation in conditions
of geographical isolation
(allopatric speciation)
Third
Mass
extinctions
Loss of species and
higher taxa
Ca. 26
Myr
Not a complete picture – ignores Milankovitch cycles
Species-rich ‘Swarms’
or ‘hotspots’ within the Himalaya
Huge diversity of one genus (up to 300 species) in
an area. Many ‘neo-endemics’. Himalaya has more
such species ‘swarms’ than any other mountain area
in the world.
Pedicularis
Primula
Cremanthodium
Meconopsis
Saussurea
Saxifraga
Rhododendron
Ligularia
Gentiana
Corydalis
Pedicularis
Pedicularis oederi, Norway
Pedicularis tricolor, Sichuan
Pedicularis przewalskii, Qinghai
Pedicularis siphonantha, Bhutan
Photo:
Mike Grant
Pedicularis bella, Bhutan
Pedicularis decorissima, Sichuan
Meconopsis
Meconopsis discigera, Bhutan
Meconopsis horridula ssp.
racemosa, Sichuan
Meconopsis horridula ssp.
horridula, Tibet
Meconopsis integrifolia
Sichuan
Meconopsis pseudointegrifolia
Yunnan
Meconopsis simplicifolia
Tibet
Meconopsis punicea
Sichuan
Meconopsis lancifolia
Sichuan
Meconopsis delavayi
Yunnan
Meconopsis aculeata
NW India
Meconopsis speciosa
Yunnan
Meconopsis
pseudovenusta, Yunnan
Meconopsis
quintuplinervia, Sichuan
Meconopsis tibetica, Tibet
Rediscovered in
2005 and described
in 2006
Many of these highly localised species-rich swarms
are in high mountain areas, often of relatively
recent (Tertiary) age.
Commonest interpretation is that these ‘swarms’
are caused by rapid habitat isolation resulting
from isolation as the land is uplifted. Combined
with locally changing conditions, result is
allopatric speciation in a small area.
Alternative hypothesis: these speciation patterns
occurred, in part at least, as a result of changing
UV-radiation experienced by the plants as the
landmass was uplifted. Provides a sympatric
speciation mechanism, or at least a mechanism
that does not require total geographical isolation.
Such isolation does not exist in places like Tibetan
Plateau – very uniform landscape and topography.
0.4
0.2
Isolation effect more and
more important at high
altitudes above 5000 m. Also
high UV-B radiation.
0.0
Ratio of endemics
0.6
Ratio of Himalayan
endemics to total species
richness steadily increases
with altitude.
0
1000
2000
3000
4000
5000
6000
Altitude
Saussurea bhutkesh
Rheum nobile
UV-B has varied in the past, related to Milankovitch
orbital mechanisms, as well as varying spatially.
More variation at high latitudes due to lower sun
angles and lower radiation values.
Over last 250 thousand years, UV-B is calculated to
have varied from -26% less to +32% more than
today.
March equinox 60°N
-10% to +12%
variation
Willis et al. (2009)
What are the biological responses
to changing UV-B over time?
UV-B changes with altitude and the formation
of ‘dwarf forest’ at the upper limit of tropical
mountain cloud forest may be related to UV-B
Stunted tree growth
Small thick leaves
Extra pigments
But no evidence for dwarf
forest in last glacial
period
Photos: Bill Baker
If temperatures
decreased but UV-B
stayed the same, climate
too cold for trees to be in
the UV-B zone, hence no
dwarf forest.
(TMCF = tropical
montane cloud forest)
Flenley (1993)
Is there a relation between increased UV-B,
diversity, and speciation?
Only one fossil record to indicate UV-B changes
through time, but only in Holocene.
Look at effect of increased UV-B related to
mountain uplift in Deep-Time.
Amount of UV-B received at a point on Earth is
mainly determined by distance from the sun.
Changes in UV-B amount can result from
latitudinal/longitudinal tectonic plate movement or
altitudinal movement (mountain uplift).
UV-B gets stronger by about 15% per km
vertically.
Qinghai-Tibet Plateau, 5000 m elevation
Uplifted in last 120 Myr as a result of collision of
Indian subcontinental plate with Eruasian plate.
Can calculate UV-B
change as Tibetan
Plateau uplifted:
increased by
approximately 100%
- twice as much UV-B
at 5000 m than at
sea-level 50 Myr ago
Willis et al. (2009)
Tibetan Plateau is centre for several swarms
of neo-endemic species
Saussurea – over 250 endemic species
Ligularia-Cremanthodium-Parasenecio – 200
endemic species
Nannoglottis – 80 endemic species
Ligularia
sagitta
Parasenecio deltophyllus
Cremanthodium
bruneopilosum
Saussurea
250
endemic
spp.
superba
bhuktesh
brunneopilosa
tangutica
medusa
Saussurea
gossipiphora
Saussurea gnaphaloides
(6400 m)
Photos: Toshio Yoshido
Saussurea
tridactyla
Molecular phylogeny of Saussurea in Qinghai shows
series of ‘bursts of diversification’ associated in
time with stages in uplift of Tibetan Plateau and then
explosive species radiation in last 20 Myr.
Similar picture for other Tibetan plants, for Andean
mountain plants, and for mountain mosses and
liverworts.
Perhaps during intervals of uplift, increased UV-B
radiation (up to 100% greater than present)
associated with the uplift may have caused significant
changes to plant populations through an increase in
mutation rates. leading to molecular evolution and
ultimately speciation.
Linked to this, increased UV-B would influence
growth responses, leading to the development of
distinctive plant morphological types.
Higher the altitude, the more times populations in
the landscape would have undergone these
processes.
May explain the increase in the proportion of
endemic plant species with altitude in the Himalaya
and the Chinese mountains.
Possible that UV-B may have had effects
disproportionately large relative to the amount of
incoming UV-B radiation, as most incoming
radiation is visible or infra-red.
Recent attempts at reconstructing changes
in UV-B flux through the Holocene
Willis et al. (2011) New Phytologist 192: 553-550
Measured para-coumaric acid
in Pinus pollen as a proxy for
recording UV-B influx through
time
Model simulation
Modern
Fossil
Now replicated at a site in Scotland
Exciting potentialities if we can reconstruct
changes in UV-B flux beyond the Holocene
(Magri 2011) in terms of understanding
variations in ozone, of environmental impacts,
and of evolution
1. Climate
2. Environment
3. Evolution
1. Climate – UV-B reconstructions may help infer
variations of ozone in the stratosphere and their
effects on climate
Increased solar activity  increased UV-C
radiation  photochemical formation of ozone
and hence adsorption of UV-B radiation
Past solar variability reconstructed using
cosmogenic solar radionuclides such as 10Be and
various biological climate proxy data
Using both solar and climate proxies, possible
connections between solar activity and climate
can be found. UV-B reconstructions make these
connections possible at 101-103 yrs, including the
possible role of human activity on climate
2. Environment – UV-B changes have many
different direct and indirect effects on terrestrial
and aquatic ecosystems
Tendency to reduce biomass accumulation. May
have impacts on community composition and
biological turnover
3. Evolution – Changes in UV-B may induce
mutations and can be expected to influence all
aspects of plant genetics up to and including
speciation rates and hence the mode and tempo
of evolution
Permian mass extinction
Increased speciation rates in Eocene and Miocene
may be association with high UV-B values
No means of currently testing them
Need fossil pine pollen covering 104-107 yrs to
test these ideas
Why is Pollen Yellow?
Flenley (2011) J. Biogeography 36: 809-816
Pine pollen floating at shore of lake in April-May –
why is it yellow?
Yellow colour results from flavonoids including
anthocyanins
• consist of three linked carbon atom rings (one
heterocyclic)
• can all absorb UV-B radiation
• pollen contains DNA for transmission to next
generation
Flavonoids could protect the DNA in pollen against
UV-B induced mutagenesis.
Why are there so Many Species in the
Tropical Rain Forest?
Flenley (2011)
A ‘big’ question in ecology and biogeography
Tropical mountain vegetation experiences highest
UV-B radiation of any vegetation type in the world.
UV-B enhanced by volcanic eruptions releasing
aerosols.
Seen that there was strong volcanicity and
mutation in late Permian
Palynological richness (& biodiversity) shows rapid
increase in Palaeocene-Eocene and early Miocene,
both times of peak temperatures
DNA phylogenies show increasing diversity at
these times
Milankovitch cycles would have caused vertical
migrations of tree taxa over about 800 m
These migrations could have led to isolation of
mountain peaks, allowing allopatric speciation,
especially in the montane elevated UV-B
environment
Process when repeated many times could lead to a
‘species pump’ and thus to high biodiversity.
Explains genera with so many species, e.g.
Rhododendron, Espeletia, and Cymbidium
New Tertiary montane volcanic UV-B hypothesis for
tropical mountain biodiversity
1. Pollen needs protection from UV-B radiation
2. UV-B radiation is mutagenic
3. UV-B radiation increases with altitude
4. Tropical mountains experience highest UV-B
radiation of any world vegetation type
5. Several tropical montane genera show isolated
species occurrences in isolated mountains
(endemic species)
6. Erupting volcanoes release SO2 and other aerosols
that destroy ozone and thus increase UV-B
radiation
7. The aerosols are active near their source and spread
widely
8. Tropical regions have many volcanoes
9. In the Permian, evidence for strong volcanism
associated with mutagenesis, presumably by UV-B
10. Volcanicity is associated with orogeny
11. Last great orogeny was the Alpine which started in
Eocene and was also active in early Miocene
12. Palynological richness shows rapid increases in
Palaeocene-Eocene and early Miocene
13. Branching of DNA trees of tropical families occurs
especially in the Palaeocene-Eocene and early
Miocene
14. Milankovitch cycles would have produced vertical
migrations of tropical taxa with a magnitude ~800m
Eocene warm phase of
Milankovitch cycle
Eocene cool phase of
Milankovitch cycle
Flenley (2011)
Wonderful example of creative lateral thinking
across disciplines
CONCLUSIONS
1. Quaternary palaeobiological data source of
information not only about past flora, vegetation,
and environment, but also populations, past
distributions, and biodiversity.
2. Plants respond to environmental change in
different ways – persistence, adaptation,
migration, extinction.
3. Migration is the dominant plant response to
Quaternary climate changes.
4. Stasis, surprisingly, is the dominant evolutionary
pattern in the Quaternary.
5. Both macro- and micro- (cryptic) refugia are
essential in both cold and temperate phases
for trees and arctic-alpine plants.
6. Speciations and extinctions surprisingly
rare in the Quaternary, other than extinctions
due to human activity.
7. Much remains to be done before ancient DNA
can be used to help test ideas about the
evolutionary legacies of the Ice Ages.
8. UV-B radiation is likely to be a major driver
of speciation but much to be learnt about how
UV-B has changed over time.
9. Quaternary palaeobiology, phylogeography,
Deep-Time palaeobiology, and biogeography
have much to contribute to our understanding
basic questions of biodiversity changes in
space and time and to assessing the
evolutionary legacies of the Ice Ages.
10. Given the complexity of biological responses
to climatic changes such as the Ice Ages seen
in the fossil record, which range from singletaxon responses to multi-taxon responses, not
surprising we are a long way from
understanding the evolutionary legacies
of the Ice Ages.
Single-taxon and
multi-taxon
responses to
climatic changes
as seen in the
mammal fossil
record. Arrows
represent
processes that link
different
responses (e.g.
range shift 
immigration 
biotic turnover)
Blois & Hadly (2009)