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Can Patterns of Ranavirus Emergence be
Used to Assess Conservation Threat?
Trent Garner, IoZ
trent.garner@ioz.ac.uk
From the GAA……
How do you classify a species as threatened?
• IUCN says (2001 IUCN Red List Categories and Criteria
version 3.1):
Critica...
• I say (Garner 2013, beta version):
Who the &*$! has all those data?
How do you classify a species infected with
ranaviru...
Theory predicts EIDs shouldn’t be bad forever
• Matching alleles, gene-
for-gene and mixed
evolutionary models for
host pa...
Evidence of host/rv (co)evolution
• ATV has been distributed
throughout western North
America through the bait trade
• Iso...
The model amphibian system
• Sonoran tiger salamander
• 30 breeding ponds in San Rafael Valley, Arizona,
a few in Mexico
•...
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 ass...
Ranavirus in the UK
• Ranavirus in UK populations are
novel, emerging since 1980s
• Dead frogs exhibited superficial
lesio...
Emergent, spreading and likely novel
FMP d-base, Stephen Price, maps
The amphibian response measured using population
genetics: evidence of sexual selection
• Populations experiencing prolong...
The amphibian response measured using population
genetics: evidence of sexual selection
• Simulations incorporating
assort...
The amphibian response measured using population
genetics: evidence of natural selection
• MHC Class 1 previously shown to...
What happens to frog populations after
emergence?
• In many cases emergence does not result in sustained
disease (about 40...
Persistent disease driven declines
• Populations experiencing
persistent disease
emergence declined
precipitously (median
...
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 1...
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 prob...
Thanks to good friends
Jaime Bosch
Amanda Duffus
Andrew
CunninghamStephen Price
Richard Nichols Amber Teacher
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Can patterns of ranavirus emergence be used to assess conservation threat?

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2013 International Symposium on Ranaviruses
by Trent Garner

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Can patterns of ranavirus emergence be used to assess conservation threat?

  1. 1. Can Patterns of Ranavirus Emergence be Used to Assess Conservation Threat? Trent Garner, IoZ trent.garner@ioz.ac.uk
  2. 2. From the GAA……
  3. 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. 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. 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. 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. 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. 8. Brunner, Schock, Davidson & Collins 2004 Ecology Intraspecific Reservoir Model
  9. 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. 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. 11. Emergent, spreading and likely novel FMP d-base, Stephen Price, maps
  12. 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. 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. 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. 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. 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. 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. 18. Multihost declines on the Continent
  19. 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. 20. Thanks to good friends Jaime Bosch Amanda Duffus Andrew CunninghamStephen Price Richard Nichols Amber Teacher

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