Species-level varia-on in ranavirus suscep-bility Jason Hoverman - - PDF document

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3/20/16 Species-level varia-on in ranavirus suscep-bility Jason Hoverman Purdue University, Department of Forestry and Natural Resources Field survey of ponds in California Bay area of California 88 total wetlands <2 ha <2 m

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3/20/16 1

Species-level varia-on in ranavirus suscep-bility

Jason Hoverman

Purdue University, Department of Forestry and Natural Resources

Field survey of ponds in California

88 total wetlands

  • <2 ha
  • <2 m deep
  • Fishless
  • Bio-c variables
  • Abio-c variables
  • Landuse

Bay area of California

Pseudacris regilla n = 627 Lithobates catesbeianus n = 123 Anaxyrus boreas n = 219 Taricha torosa n = 464 Taricha granulosa n = 125

Infection prevalence

Positive individuals American bullfrog Boreal toad Pacific chorus frog Rough skinned newt California newt 0% 10% 20% 30% 40% 50% 60% Infected (%)

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3/20/16 2

Field surveillance of ponds in Tennessee

Cumberland Plateau TN River Ridge & Valley 40 Sites

33 of 40 sampled ponds (83%) Prevalence ≥ 40% in 13 ponds (39%) Detected across mul-ple seasons in 20 ponds (61%) 9 of 13 species tested posi-ve (69%)

Infec-on prevalence

American toad

  • E. narrow-mouthed toad
  • N. cricket frog

Gray tree frog Upland chorus frog Pickerel frog

  • S. leopard frog

Bullfrog Green frog Mole salamander Tiger salamander Red spotted newt Desmog 10 20 30 40 50 60 70 80 90 Infected (%)

32 26 22 21 62 145 18 327 377 13 8 157 2

10 20 30 40 50 60 70 80 90 Number infected

Ranids were the most frequently infected group Varia-on in infec-on prevalence among species Only 63% of species at a site tested posi-ve

Summary of field paZerns

Ranavirus is common but there is varia<on

  • Infec<on prevalence varies among species/groups
  • All species at a site are not infected despite the

presence of ranavirus Inferring suscep<bility from field data is difficult

  • Bias in sampling
  • Exposure history
  • Confounding environmental variables
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3/20/16 3 Varia-on in disease outcomes

Co-occurring host species oLen differ in:

  • Infec<on
  • Pathology

Varia<on is a product of:

  • Phylogeny
  • Ecology
  • Life history

Exploring the influence of these factors on disease

  • utcomes is a major step towards predic<ng disease

risk within natural systems

Pace-of-life con-nuum

Life history axis: variation between species/ populations: Reproduction: slow Survival: high “Slow-living” Development time: long Survival: low Reproduction: fast Development time: short “Fast-living” Life history axis: Individual variation: Higher intensity of effort (reproductive or other) Lower intensity effort More demanding season Less demanding season Sex investing more in an activity Sex investing less in an activity Less specific and/or more inflammatory Induced immune defense axis: Minimize autoimmune costs, maximize longevity: Adaptive immunity Th2 rather than Th1 Minimize conflicts with rapid reproduction: Innate immunity Th1 emphasis Constitutive immune defense axis: More specific, less inflammatory Less constitutive More constitutive Pathogen exposure axis: More frequent Less frequent More extracellular (e.g., some bacteria, macroparasites) More intracellular (e.g., viruses)

Lee 2006; Integra8ve and Compara8ve Biology

Examples

Lee et al 2008; J Animal Ecol

  • Fig. 2. Relationship between incubation period and estimates of

natural antibody titre (measured as haemagglutination) across tropical bird species. Data points are species means; the line represents a conventional linear model fit.

Tropical birds

–2.5 –2.0 –1.5 –1.0 –0.5 0.0 0.5 1.0 5 10 15 20 25 30 Vector population size (a) –2.5 –2.0 –1.5 –1.0 –0.5 0.0 0.5 1.0 0.0 0.2 0.4 0.6 0.8 1.0 Susceptibility (prob. of infection)

134 99 100 12 15 90 (d)

–2.5 –2.0 –1.5 –1.0 –0.5 0.0 0.5 1.0 0.0 0.2 0.4 0.6 0.8 1.0 Competence (prob. of acquisition) Principal component axis 1 (physiological phenotype)

6 3 9 75 45 10 (g)

Plants

Cronin et al 2010; Ecol Le@ers

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3/20/16 4 Approach

Let’s apply this framework to amphibians

  • Collect as many species as possible
  • Under controlled condi<ons exposure them to ranavirus and

assess disease outcomes

  • Infec<on
  • Mortality
  • Use phylogene<c methods to assess the rela<ve importance
  • Phylogeny
  • Ecology
  • Life history

Species collec-on

Ranidae (7)

Wood frog Gopher frog Southern leopard frog Northern leopard frog Pickerel frog American bullfrog Green frog

Hylidae (4)

Cope’s gray tree frog Western chorus frog Upland chorus frog Mountain chorus frog

Other anurans (3)

American toad Eastern narrow-mouthed toad Eastern spadefoot

19 species from 7 families tested

Ambystoma-dae (4)

Mole salamander Tiger salamander Spo`ed salamander Marbled salamander

Salamandridae (1)

Red-spo`ed newt

The experiments

Mortality and infec<on prevalence

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3/20/16 5

Results Species results

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t e d n e w t 2 4 6 8 10 12 14 16 18 20 Number of individuals Died, infected Survived, infected Died, not infected Control

Species results

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d T i g e r s a l a m a n d e r M a r b l e d s a l a m a n d e r S p

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t e d n e w t 2 4 6 8 10 12 14 16 18 20 Number of individuals Died, infected Survived, infected Died, not infected Control

High survivorship and no infec<on in control animals

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3/20/16 6

Species results

Broad host range with varia<on in disease outcomes

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t e d n e w t 2 4 6 8 10 12 14 16 18 20 Number of individuals Died, infected Survived, infected Died, not infected FV3

* * * * * * * * *

Species results

Broad host range with varia<on in disease outcomes

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t e d n e w t 2 4 6 8 10 12 14 16 18 20 Number of individuals Died, infected Survived, infected Died, not infected Ranaculture isolate

Phylogene-c compara-ve methods

0.0 50.0 100.0 150.0 200.0 250.0 300.0 Pickerel frog Wood frog Southeastern chorus frog Western chorus frog Tiger salamander Gopher frog Mountain chorus frog Marbled salamander Cope’s gray treefrog American toad Northern leopard frog Green frog Eastern spadefoot Southern leopard frog Mole salamander Spotted salamander American bullfrog Eastern narrow-mouthed toad Red-spotted newt

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3/20/16 7

Family-level paZerns in suscep-bility

Ranids were generally the most suscep<ble to infec<on

Ambystomatidae Hylidae Ranidae 10 20 30 40 50 60 70 80 90 Infection prevalance (%) FV3 Ranaculture isolate

(K = 0.430, Z = -0.567, P = 0.298) Species-level traits (9) Breeding habitat Breeding <me Dura<on of larval stage (d) Size at metamorphosis (mm) Clutch size Dura<on of egg stage (d) Adult body size (mm) Time to maturity (yr) Species range (km2)

Are there associa<ons between species traits and suscep<bility?

0.0 50.0 100.0 150.0 200.0 250.0 300.0 Pickerel frog Wood frog Southeastern chorus frog Western chorus frog Tiger salamander Gopher frog Mountain chorus frog Marbled salamander Cope’s gray treefrog American toad Northern leopard frog Green frog Eastern spadefoot Southern leopard frog Mole salamander Spotted salamander American bullfrog Eastern narrow-mouthed toad Red-spotted newt

Phylogene<c independent contrasts Phylogene<c generalized least squares

Phylogene-c compara-ve methods Ecology and suscep-bility

Breeding habitat (r = 0.490, n = 17, P = 0.046 )

Temporary Semi-permanent Permanent 10 20 30 40 50 60 70 80 90 Infection prevalance (%)

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3/20/16 8

Life history and suscep-bility

Dura<on of larval stage (Pearson’s r = -0.460, n = 18, P = 0.046)

  • 6
  • 4
  • 2

2 4 6 8 10

  • 0.08
  • 0.06
  • 0.04
  • 0.02

0.02 0.04 0.06 Infection prevlance contrasts Time to metamophosis contrasts

Including addi-onal species

2 4 6 8 10 12 14 16 18 20 Number of individuals Died not infected Survived infected Died infected 2 4 6 8 10 12 14 16 18 20 Number of individuals 2 4 6 8 10 12 14 16 18 20 Number of individuals

Control FV3 RI A C B

16 species added to the list Same general patterns found

FV3 RI

Pace-of-life with amphibian parasites

Metacercarial load (arcsine square root) AMMA TATO XELA RACA RAPR LICA LISY ANBO ANAM HYVE HYCH PSRE PSTR –1.5 –1.0 –0.5 0.0 0.5 1.0 1.5 2.0 2.5 3.0 0.00 0.10 0.20 0.30 0.40 0.50 0.60 0.70 0.80 AMMA TATO XELA RACA RAPR LICA LISY ANBO ANAM HYVE HYCH PSRE PSTR P = 0.0105; r2 = 0.535 Natural log mortality odds AMMA TATO XELA RACA RAPR LICA LISY ANBO ANAM HYVE HYCH PSRE PSTR –1.5 –1.0 –0.5 0.0 0.5 1.0 1.5 2.0 2.5 3.0 –0.01 0.00 0.01 0.02 0.03 0.04 0.05 0.06 0.07 0.08 AMMA TATO XELA RACA RAPR LICA LISY ANBO ANAM HYVE HYCH PSRE PSTR P = 0.0072; r2 = 0.571 Factor 1 (pace of life) Natural log malformation odds AMMA TATO XELA RACA RAPR LICA LISY ANBO ANAM HYVE HYCH PSRE PSTR –1.5 –1.0 –0.5 0.0 0.5 1.0 1.5 2.0 2.5 3.0 –0.04 0.00 0.04 0.08 0.12 0.16 0.20 0.24 0.28 AMMA TATO XELA RACA RAPR LICA LISY ANBO ANAM HYVE HYCH PSRE PSTR P = 0.0191; r2 = 0.474 (a) (b) (c)

The trematode Ribeiroia ondatrae Fast-paced species had:

  • Greater parasite loads
  • Greater probability of mortality
  • More malforma<ons

Figure 3 Relationships between Factor 1 from the factor analysis (pace-of-life axis) and responses variables: (a) parasite load at metamorphosis (arcsine-square root transformed); (b) mortality risk (ln-transformed odds ratio); (c) malformation risk (ln-transformed odds ratio). Trendlines and associated statistics plotted for each panel with H. versicolor and H. chyrsoscelis excluded. For ease of presentation, graphs reflect data without correcting for phylogenetic relationships (see text for details). Johnson et al. 2012. Eco Letters

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3/20/16 9

Summary

Species-level varia<on in suscep<bility is not random

  • Phylogeny – shared evolu<onary history
  • Ecology – habitat preferences that influence exposure
  • Life history – Pace-of-life con<nuum
  • ‘Fast-lived’ species with rapid growth and short life spans

invest li`le in pathogen defense

  • ‘Slow-lived’ species with slow growth and long life spans

invest more in pathogen defense

Varia-on among other ectotherms

Fish and turtle species have been examined for suscep<bility to different ranavirus isolates

10 20 30 40 50 60 70 80 90 100 Individuals (%) Died not infected Survived, infected Died infected 10 20 30 40 50 60 70 80 90 100 Individuals (%) 10 20 30 40 50 60 70 80 90 100 Individuals (%) 10 20 30 40 50 60 70 80 90 100 Individuals (%) 10 20 30 40 50 60 70 80 90 100 Control Turtle Fish Amphibian Individuals (%) Isolate

Channel Catish Nile Tilapia Western Mosquitoish Fathead Minnow Bluegill

10 20 30 40 50 60 70 80 90 100 Individuals (%) Survived, infected Died, not infected Died, infected 10 20 30 40 50 60 70 80 90 100 Individuals (%) 10 20 30 40 50 60 70 80 90 100 Control Turtle Fish Amphibian Individuals (%) Isolate Eastern river cooter Florida softshell turtle Mississippi map turtle

Brenes et al. 2014. J of Aqua8c Animal Health

Immune func<on decreases during metamorphosis Suscep<bility to pathogens should be highest at metamorphosis Individuals near metamorphosis are frequently reported in die-off events

Nathan Haislip

Influence of development on suscep-bility

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3/20/16 10

Experimental approach

Does suscep<bility vary across developmental stages?

Exposed to the virus for 3 days at each stage and moved to clean water

Results

  • Variable pa`erns across

species

  • Metamorphic stages are

not universally the most suscep<ble

  • Eggs are generally

protected from infec<on

Haislip et al. 2011 PLoS ONE