2013 International Symposium on Ranaviruses by Trent Garner

1. Can Patterns of Ranavirus Emergence be
Used to Assess Conservation Threat?
Trent Garner, IoZ
trent.garner@ioz.ac.uk

2. From the GAA……

3. 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

4. • I say (Garner 2013, beta version):
Who the &*$! has all those data?
How do you classify a species infected with
ranavirus as threatened?

5. 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.

6. 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

7. 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…….

8. Brunner, Schock, Davidson & Collins 2004 Ecology
Intraspecific Reservoir Model

9. 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

10. 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

11. Emergent, spreading and likely novel
FMP d-base, Stephen Price, maps

12. 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

13. 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

14. 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

15. 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……….

16. 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

17. Little evidence of viral evolution or expanded host
range
0
10
20
30
40
50
60
70
80
90
100
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30
Control
BUK 2 10^4
BUK 2 10^6
BUK 3 10^4
BUK 3 10^6
RUK 1110^4
RUK 1110^6
RUK 13 10^4
RUK 13 10^6
7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30
Control
BUK 2 10^4
BUK 2 10^6
BUK 3 10^4
BUK 3 10^6
RUK 1110^4
RUK 1110^6
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 13 104
Survival(%)
Time (Days)
A.L.J. Duffus unpubl. data

18. Multihost declines on the Continent

19. 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

20. Thanks to good friends
Jaime Bosch
Amanda Duffus
Andrew
CunninghamStephen Price
Richard Nichols Amber Teacher