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 deep • Fishless • Bio-c variables • Abio-c variables • Landuse Infection prevalence Positive individuals Pseudacris regilla Lithobates catesbeianus Anaxyrus boreas Taricha torosa Taricha granulosa n = 627 n = 123 n = 219 n = 464 n = 125 0 60% 50% Infected (%) 40% 30% 20% 10% 0% American bullfrog Boreal toad Pacific chorus frog California newt Rough skinned newt 1
3/20/16 Field surveillance of ponds in Tennessee TN River Ridge & Valley Cumberland Plateau 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 90 80 70 Number infected 60 Ranids were 50 the most 40 30 frequently 20 10 infected group 0 90 80 Only 63% of species at a site 8 70 Varia-on in tested posi-ve Infected (%) 60 infec-on 50 40 prevalence 30 377 20 22 18 among species 145 327 10 157 32 62 26 21 13 2 0 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 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 2
3/20/16 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 outcomes is a major step towards predic<ng disease risk within natural systems Pace-of-life con-nuum Life history axis: “Slow-living” “Fast-living” variation between Reproduction: slow Reproduction: fast species/ populations: Development time: long Development time: short Survival: low Survival: high Life history axis: Lower intensity effort Higher intensity of effort Individual (reproductive or other) variation: Less demanding season More demanding season Sex investing more in an Sex investing less in an activity activity Minimize autoimmune costs, Minimize conflicts with Less specific More specific, maximize longevity: rapid reproduction: and/or more less Induced immune inflammatory Adaptive immunity inflammatory Innate immunity defense axis: Th2 rather than Th1 Th1 emphasis Constitutive Less constitutive More constitutive immune defense axis: More extracellular (e.g., some bacteria, macroparasites) More intracellular (e.g., viruses) Pathogen exposure axis: More frequent Less frequent Lee 2006; Integra8ve and Compara8ve Biology Examples Plants Tropical birds 30 (a) 25 Vector population size 20 15 10 5 0 –2.5 –2.0 –1.5 –1.0 –0.5 0.0 0.5 1.0 1.0 Susceptibility (prob. of infection) (d) 100 0.8 15 12 0.6 90 0.4 0.2 134 0.0 99 –2.5 –2.0 –1.5 –1.0 –0.5 0.0 0.5 1.0 Competence (prob. of acquisition) 1.0 (g) 10 75 0.8 45 9 0.6 3 0.4 6 0.2 Fig. 2. Relationship between incubation period and estimates of natural antibody titre (measured as haemagglutination) across tropical 0.0 bird species. Data points are species means; the line represents a –2.5 –2.0 –1.5 –1.0 –0.5 0.0 0.5 1.0 Principal component axis 1 (physiological phenotype) conventional linear model fit. Lee et al 2008; J Animal Ecol Cronin et al 2010; Ecol Le@ers 3
3/20/16 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 19 species from 7 families tested Ranidae (7) Other anurans (3) Wood frog American toad Gopher frog Eastern narrow-mouthed toad Southern leopard frog Eastern spadefoot Northern leopard frog Pickerel frog Ambystoma-dae (4) American bullfrog Mole salamander Green frog Tiger salamander Spo`ed salamander Hylidae (4) Marbled salamander Cope’s gray tree frog Western chorus frog Salamandridae (1) Upland chorus frog Red-spo`ed newt Mountain chorus frog The experiments Mortality and infec<on prevalence 4
Number of individuals Number of individuals W 10 12 14 16 18 20 W 10 12 14 16 18 20 o 0 2 4 6 8 o 0 2 4 6 8 o o d d f f r o r o S G g S G g o o o o p p u u t h h t h h e e High survivorship and no infec<on in control animals e e r r r n f r n f r o r o N l e g N l e g o o o o r p r p t h a t h a e r e r d d r n f r n f r o r o l e l e g g o o p Died, infected p Died, infected a a r r d d f f r r P o P o i g i g c c k k e e r e r e l l f r f r o o g g G G r r e e A e A e m n m n e f r e f r r i o r i o C c g C c g a a o n Species results o n Species results p p e b e b ' u ' u s l l s l l g f r g f r r o r o a g a g W y W y e t r e t r s e s e t e t e e e r f r r f r n o n o c g c g Results h h U o U o p r u p r u l l a s Survived, infected a s Survived, infected n f n f d r o d r o M c g M c g h h o o o o u r u r n u n u t s t s a f a f n i r i n r o o c g c g h h o o r r u u s s A A f r f r m o m o e g e g r r i i E c E c a a a a s n s n t t t t e o e o r a r a N n d N n d a s a s r p r p r a r a o o w d w d - e - e m f o m f o o o o o u t u t t h t h T e T e i g d i g d t t e o e o r a r a s d s d M a M a l l a a a a r m r m b a b a l e e l d n Died, not infected d n Died, not infected d d s e s e a r a r S l S l p a p a o m o m t t t e a t e a n n d d d d s e s e a r a r l l a a m m M M o a o a l n l n e d e d e e s r s r a a l a l a R m R m e a Control e a Control d n d n - d - d s e s e p p o r o r t t t e t e d d n n e e w w t t 3/20/16 5
3/20/16 Species results Broad host range with varia<on in disease outcomes Died, infected Survived, infected Died, not infected 20 FV3 18 Number of individuals 16 14 12 10 8 6 4 2 0 g g g g g g g g g g g d t d r r r r t o e e e w o o o o o o o o o o o a a e o d d d r r r r r r r r r r r o o d e f f f f f f f f n n n f f f l f t e t n n r d d l n l e s s a a a d e e u s n d d a r r e e u u u m m m d o h r b a a e m a a e e r r r r e o p t o o o c p h a a a a W p p k r n t o G y h h h i s t l l l l t o o c a r u a a a a o G a c c c e p * e e i * c n o s s s s P i r m s l l * r g n d n r m n n e e r d d e - r n i A e d r r m s e a t - e e l e e a s w g o e ' t t l t h h A e s l n a T i b t M R p o o t t * p e u E * r u r U r a p * o W o r o o a M S C M S N N * * * Species results Broad host range with varia<on in disease outcomes Died, infected Survived, infected Died, not infected 20 Ranaculture 18 isolate 16 Number of individuals 14 12 10 8 6 4 2 0 g g g g g g g g g g g d t d r r r r t o e e w o o o o o o o o o o o a a e e o d d d r r r r r r r r r r r o o d e f f f f f f f f f n n n f f l f t e t n n d r d l n l e s s a a a d e u s n d d a o e r e e u u u m m m d a r r b a a e m o h a e e r r r r e p o o o c p h a a a a W p p k r n t t o h h h i s t l l l l t o o c G a y r u a a a a o e a c c c e G e i c n o s s s s p l P r m l r i g n d n r m s n n e r d d e - e r n i A e r r s e a t - e e l d e m a s w g o e ' t t b l t e h A e s l n a i t M h p o T r o R t t p e u E u r U r a p o W o r o o a M S C M S N N Phylogene-c compara-ve methods Mole salamander Spotted salamander Tiger salamander Marbled salamander Red-spotted newt Eastern spadefoot Eastern narrow-mouthed toad Wood frog Green frog American bullfrog Northern leopard frog Southern leopard frog Gopher frog Pickerel frog Cope’s gray treefrog Mountain chorus frog Southeastern chorus frog Western chorus frog American toad 300.0 250.0 200.0 150.0 100.0 50.0 0.0 6
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