can patterns of ranavirus emergence be used to assess conservation threat?
DESCRIPTION
2013 International Symposium on Ranaviruses by Trent GarnerTRANSCRIPT
Can Patterns of Ranavirus Emergence be
Used to Assess Conservation Threat?
Trent Garner, IoZ
From the GAA……
How do you classify a species as threatened?
• IUCN says (2001 IUCN Red List Categories and Criteria
version 3.1):
Critically Endangered: big reduction in population size (>80%), geographic
range 10-100 km2 and suffering from severe fragmentation, loss of habitat,
decline in extent of occurrence, etc., population size 50-250 individuals and
declining, with 50% risk of extinction in 10 years
Endangered: reduction in population size (>50%), geographic range 500-
5000 km2 and suffering from fragmentation, loss of habitat, decline in
extent of occurrence, etc., population size 250-2500 individuals and
declining, with 20% risk of extinction in 20 years
Vulnerable: reduction in population size (>30%), geographic range 2000-
20000 km2 and suffering from fragmentation, loss of habitat, decline in
extent of occurrence, etc., population size 1000-10000 individuals and
declining, with 10% risk of extinction in 100 years
• I say (Garner 2013, beta version):
Who the &*$! has all those data?
How do you classify a species infected with ranavirus as threatened?
Theory predicts EIDs shouldn’t be bad forever
• Matching alleles, gene-
for-gene and mixed
evolutionary models for
host parasite dynamics
do NOT predict host
extinction
• As long as host evolution
facilitates response to
the parasite, the host
should be able to defend
against parasite intrusion
Agrawal & Lively 2002 Evol. Ecol. Res.
Evidence of host/rv (co)evolution
• ATV has been distributed
throughout western North
America through the bait trade
• Isolates of ATV exhibit
stabilizing selection at elF-2α,
caspase activation and
recruitment domain and
directional selection β-OH-
steroid oxidoreductase genes
Ridenhour & Storfer 2008 Journal of Evolutionary Biology
Pearman & Garner 2005 Ecology Letters
• Tadpoles sourced from Rana
latastei populations with
varying neutral genetic
diversity challenged with FV3
• Tadpoles from low diversity
populations were
comprehensively killed, those
from high diversity
populations fared far better
• Lineage effects
The model amphibian system
• Sonoran tiger salamander
• 30 breeding ponds in San Rafael Valley, Arizona,
a few in Mexico
• Epizootics first observed in 1985, thought to be
caused by bacteria
• Virus isolated in late 90s (Jancovich et al. 1997 DAO),
Koch’s postulates satisfied, named ATV
• Epizootics continue, no evidence of host
extirpation at any breeding pond
• The model…….
Brunner, Schock, Davidson & Collins 2004 Ecology
Intraspecific Reservoir Model
Does the IRM really indicate there is no problem?
• Lack of ‘pretreatment’ data
• Population maintenance under the IRM assumes single
stage (larval) density dependent transmission
• Amphibian populations commonly subject to multi-
stage density-dependent regulation (Hellreigel 2000 Oikos)
• Single host species system
Ranavirus in the UK
• Ranavirus in UK populations are
novel, emerging since 1980s
• Dead frogs exhibited superficial
lesions and internal haemorrhages
• Dozens of dead animals at a site,
sometimes hundreds
• Data are contributed by the public
and predominantly based on
observations at garden ponds
Gory pictures courtesy of Amanda Louise Jean Duffus
Emergent, spreading and likely novel
FMP d-base, Stephen Price, maps
The amphibian response measured using population genetics: evidence of sexual selection
• Populations experiencing prolonged disease emergence exhibit
some evidence for decreased heterozygosity, but consistent
evidence of increased FIS and decreased relatededness after
correcting for inbreeding
• No evidence of bottlenecks
Teacher et al 2009 Molecular Ecology
The amphibian response measured using population genetics: evidence of sexual selection
• Simulations incorporating
assortative mating could
recover similar values for
population genetics
parameters
• e.g., FIS
Teacher et al 2009 Molecular Ecology
The amphibian response measured using population genetics: evidence of natural selection
• MHC Class 1 previously shown to be important in
host immune response to ranavirus infection
• MHC Class 1a is a single locus in R. temporaria
• Rv+ and Rv- pops share expressed alleles, but
nucleotide diversity higher in Rv- populations
• the frequency of supertypes (23 in total) differed on
the basis of population disease status
Teacher et al 2009 PLoS ONE
What happens to frog populations after emergence?
• In many cases emergence does not result in sustained
disease (about 40%)
• About 10% of frog populations disappear
• In the remaining populations, disease is maintained
over time……….
Persistent disease driven declines
• Populations experiencing
persistent disease
emergence declined
precipitously (median
population size change -
83%) and didn’t recover
• Size of population before
emergence did not buffer
against this, in fact the
opposite: larger
population lost
proportionately greater
numbers of frogs
Teacher et al 2010 Animal Conservation
Little evidence of viral evolution or expanded host range
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Control
BUK 2 10^4
BUK 2 10^6
BUK 3 10^4
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RUK 11 10^4
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Control
BUK 2 10^4
BUK 2 10^6
BUK 3 10^4
BUK 3 10^6
RUK 11 10^4
RUK 11 10^6
RUK 13 10^4
RUK 13 10^6
Control
BUK 2 104
BUK 2 106
RUK 11 104
BUK 3 106
BUK 3 104
RUK 11 106
RUK 13 106
RUK 13 104Surv
ival (%
)
Time (Days)
A.L.J. Duffus unpubl. data
Multihost declines on the Continent
Different rvs are in Europe
• At least 4 distinct
lineages are in Europe, 3
on the continent, one in
the UK
• All can probably kill A.
obstetricans, at least two
are serious, multihost
pathogens
• All probably introduced,
so recent (co)evolution is
out the window
Thanks to good friends
Jaime Bosch
Amanda Duffus
Andrew
CunninghamStephen Price
Richard Nichols Amber Teacher