Making the case for

Steven Hamblin and Mark TanakaUniversity of New South Wales

Viral niche construction

Boni & Feldman, 2005

... “the phenomenon of constructing, destroying, or altering one’s environment and thus changing the selection pressures exerted by that environment.”

t

t+1

Et Gene pool

Et+1 Gene pool

Populations of diverse

phenotypes

Populations of diverse

phenotypes

Gen

etic

inhe

rita

nce

Natural selection

Natural selectiontim

e

t

t+1

Et Gene pool

Et+1 Gene pool

Populations of diverse

phenotypes

Populations of diverse

phenotypes

Gen

etic

inhe

rita

nce

Natural selection

Niche construction

Ecol

ogic

al in

heri

tanc

e

Natural selection

Niche constructiontim

e

BarbetsBeech trees

Embioptera

Euchondrus

Red admiralTits

Bucerotidae

Corvids

HamstersScombridaePicidae

GastercanthaCoral

Ants

Cynomys Macronema

Lizards

Chameleons

Flow

erin

g pla

nts

Helicopsychidae

Gazelles

Cricitelus

Thrush

Lampreys

Galliwasps

Snails

Apinae

TrachinoideiFurnariidae

Theridion

Hydropsychiade

Gymnopphiona

Voles

Katydids

DeinopidaeSiluriformes

Sarcophagids

Lovebirds

Acacia

BirdsErinaceus

Hedgehogs

Viruses

Carp

Segestriidae

Cod

Storks

Hominids

Puffinus

Treehoppers

Paradise fish

Mites

Tortoise

Lobsters

Prairie dogs

Beeflies

Badgers

Coniosporium

House martin

Macrotermitinae

Sphagnum

VulpesPetromyzontiformes

Thysanoptera

Bembix Hemisotidae

Cavia

Hirundinidae

MolesVanessa

Megapodes

Caterpillars

DermapteraScolytidae

Painted lady

Drosophila

Catfish

Flies

Lepidoptera

ApodidaeJerboas

Vespinae

Sharks

Algae

Testudinata

Ploceidae

Ostariophysi

CaeliferaApicotermes

Dendrobatidae

Bees

Fishes

Reptiles

Microphytes

Tetragnatha

DiatomsSawflies

Butterflies

MyctophidaeArgyroneta

Spiders

Bats

Neanderthals

Pipesnakes

Chiromantis

Turdus Dipodidae

MerganserRiver otters

Caecilians

Porcupines

Trionychidae

Lemmings Finch

Guinea pigs

Petrel

Wasps

Lichens

Paelobatidae

Iguanas

Cuckoo

Sardines

Swifts

Eels

Smelts

Teiidae

Wildebeest

Ariadna

Mouthbrooder

Peromyscus

Psocoptera

Acrididae

Skinks

Agapornis

Fungi

Pisauridae

Gobies

Coleoptera

Buffalo grass

Arachnids

Turtles

Tuna

Honey eater

Whales

Tenebrionidae

Cichlids

Homo

Lanternfishes

Rats

Philopotamidae

Hummingbirds

Gryllotalpidae

Muskrats

Areneus Parasitoid insects

Pleurodira

Capitonidae

Myrmeleontidae

Tuatara

Meropidae

SilverfishSynbranchiformes

Trochilidae

Cattle

Typhlopidae

Gophers

Rabbits

Bowerbirds

Wombats

Sea t

urtl

e

Rodents

Liphistiidae

Ant lions

Spalax

Crocodiles

Plants

Amphipods

Mona

rch

butt

erfl

y

Snapping shrimps

Millipedes

CassavaTrichoptera Ch

aparral

Tephritid flies

Wren

Eublepharidae

Orthoptera

AttaHornbills

Locusts

Rhynchocephalia

Hymenoptera

Chiroptera

Terrapins

Earwigs

Cyclosa

Bathyergidae

Alcedinidae

Pongidae

Vombatidae

Hemiptera

Alligators

Moths

Eagles

Pythons

Termites

Lutra

Animalia

Motmots

Louse

Worms

Segestria

Uloborus

Kingfishers

Mallos

Magpies

Scincidae

Weeverfishes

MalariaOwls

Ophichthidae

Hirundines

Braconidae

Marmots

Melinae

Rooks

Dipterans

Insects

Ctenizidae

Primates

Grasses

BlattodeaWeaverbirds

Eubacteria

Epiphytes

Stickelback

Gasterosteus

Testudinidae

SnakesLeptotyphlopidae

Vipes

Toadfish

Cyanobacteria

Chough

Ergot fungus

Snake eels

Batrachoididae

Mosses

Trees

Bark lice

Viceroy

Ichneumonidae

Parus

Guppies

Teleutomyrmex

Pygopodids

Black rush

Pine trees

Congridae

Tachyoryctes

SalmonOpossum

Grasshoppers

Mosquitoes

Eumenidae

Nile monitor

Frogs

Turkeys

Clupeiformes

Gecko

Basidiomycetes

Milkweed

Dolphins

Bombyliidae

Rhinophrynidae

Eider duck

FoxesOviparous insects

Lycosidae

Characiformes

Galaxids

Hystrix

Zebras

Anomalepididae

Beavers

Flatworms

Vertebrates

Mole rats

Aniliidae

Uropeltidae

Cows

Amphibians

Helodermatidae

Osmeridae

Tapinillus

Passalidae

Isopods

Membracidae

Protists

Squirrels

Microhylidae

Momotidae

Polistinae

Eucalyptus

Dibamids

Ensiferan

Mammals

Cormorants

Stomiiformes

Cicadas

Bacteria

Braunsapis

Zooplankton

Amphisbaenia

Sauria

Scarabaeidae

Archaebacteria

Gerbils

Reithrodontomys

Beetles

Anguillidae

Cyclorana�

Dragonfishes

Periophthalmus

Woodpeckers

Ptilonorhynchidae

Sandpipers

Mudskippers

Bee eaters

Limnephilidae

Ovenbirds

Symphyta

Swallows

Crustaceans

BarbetsBeech trees

Embioptera

Euchondrus

Red admiralTits

Bucerotidae

Corvids

HamstersScombridae

PicidaeGastercantha

Coral

Ants

Cynomys Macronema

LizardsChameleons

Flow

erin

g pla

nts

Helicopsychidae

Gazelles

Cricitelus

Thrush

Lampreys

Galliwasps

Snails

Apinae

TrachinoideiFurnariidae

Theridion

Hydropsychiade

Gymnopphiona

Voles

Katydids

Deinopidae

Siluriformes

Sarcophagids

Lovebirds

Acacia

BirdsErinaceus

Hedgehogs

Viruses

Carp

Segestriidae

Cod

Storks

Hominids

Puffinus

Treehoppers

Paradise fish

Mites

Tortoise

Lobsters

Prairie dogs

Beeflies

Badgers

Coniosporium

House martin

Macrotermitinae

Sphagnum

VulpesPetromyzontiformes

Thysanoptera

Bembix Hemisotidae

Cavia

Hirundinidae

MolesVanessa

Megapodes

Caterpillars

DermapteraScolytidae

Painted lady

Drosophila

Catfish

Flies

Lepidoptera

ApodidaeJerboas

Vespinae

Sharks

Algae

Testudinata

Ploceidae

Ostariophysi

CaeliferaApicotermes

Dendrobatidae

Bees

Fishes

Reptiles

Microphytes

Tetragnatha

DiatomsSawflies

Butterflies

MyctophidaeArgyroneta

Spiders

Bats

Neanderthals

Pipesnakes

Chiromantis

Turdus Dipodidae

MerganserRiver otters

Caecilians

Porcupines

TrionychidaeLemmings Finch

Guinea pigs

Petrel

Wasps

Lichens

Paelobatidae

Iguanas

Cuckoo

Sardines

Swifts

Eels

Smelts

Teiidae

Wildebeest

Ariadna

Mouthbrooder

Peromyscus

Psocoptera

Acrididae

Skinks

Agapornis

Fungi

Pisauridae

Gobies

Coleoptera

Buffalo grass

Arachnids

Turtles

Tuna

Honey eater

Whales

Tenebrionidae

Cichlids

Homo

Lanternfishes

Rats

Philopotamidae

Hummingbirds

Gryllotalpidae

Muskrats

Areneus Parasitoid insects

Pleurodira

Capitonidae

Myrmeleontidae

Tuatara

Meropidae

SilverfishSynbranchiformes

Trochilidae

Cattle

Typhlopidae

Gophers

Rabbits

Bowerbirds

Wombats

Sea t

urtl

e

Rodents

Liphistiidae

Ant lions

Spalax

Crocodiles

Plants

Amphipods

Mona

rch

butt

erfl

y

Snapping shrimps

Millipedes

CassavaTrichoptera Ch

aparral

Tephritid flies

Wren

Eublepharidae

Orthoptera

AttaHornbills

Locusts

Rhynchocephalia

Hymenoptera

Chiroptera

Terrapins

Earwigs

Cyclosa

Bathyergidae

Alcedinidae

Pongidae

Vombatidae

Hemiptera

Alligators

Moths

Eagles

Pythons

Termites

Lutra

Animalia

Motmots

Louse

Worms

Segestria

Uloborus

Kingfishers

Mallos

Magpies

Scincidae

Weeverfishes

MalariaOwls

Ophichthidae

Hirundines

Braconidae

Marmots

Melinae

Rooks

Dipterans

Insects

Ctenizidae

Primates

Grasses

BlattodeaWeaverbirds

Eubacteria

Epiphytes

Stickelback

Gasterosteus

Testudinidae

SnakesLeptotyphlopidae

Vipes

Toadfish

Cyanobacteria

Chough

Ergot fungus

Snake eels

Batrachoididae

Mosses

Trees

Bark lice

Viceroy

Ichneumonidae

Parus

Guppies

Teleutomyrmex

Pygopodids

Black rush

Pine trees

Congridae

Tachyoryctes

SalmonOpossum

Grasshoppers

Mosquitoes

Eumenidae

Nile monitor

Frogs

Turkeys

Clupeiformes

Gecko

Basidiomycetes

Milkweed

Dolphins

Bombyliidae

Rhinophrynidae

Eider duck

FoxesOviparous insects

Lycosidae

Characiformes

Galaxids

Hystrix

Zebras

Anomalepididae

Beavers

Flatworms

Vertebrates

Mole rats

Aniliidae

Uropeltidae

Cows

Amphibians

Helodermatidae

Osmeridae

Tapinillus

Passalidae

Isopods

Membracidae

Protists

Squirrels

Microhylidae

Momotidae

Polistinae

Eucalyptus

Dibamids

Ensiferan

Mammals

Cormorants

Stomiiformes

Cicadas

Bacteria

Braunsapis

Zooplankton

Amphisbaenia

Sauria

Scarabaeidae

Archaebacteria

Gerbils

Reithrodontomys

Beetles

Anguillidae

Cyclorana�

Dragonfishes

Periophthalmus

Woodpeckers

Ptilonorhynchidae

Sandpipers

Mudskippers

Bee eaters

Limnephilidae

Ovenbirds

Symphyta

Swallows

Crustaceans

NATURE|Vol 437|15 September 2005 INSIGHT REVIEW

359

ton, where virus-infected cells sink rapidly78, potentially increasing thetransport of cells to deeper waters27. Nutrients other than carbon arealso released by viral lysis79,80. As these nutrients are largely organicallybound, this can affect their availability and pathways of cycling. Insome cases, released nutrients such as iron can fill a major portion ofthe requirements of other organisms80. As well, the small size of virusesmakes them excellent nucleation sites for mineralization of iron andperhaps other metals81.

Marine viruses and diseaseViruses are not only players in microbial mortality and geochemicalcycling, they are also progenitors of disease in higher organisms. Ourlimited knowledge of viral diseases in non-microbial marine organ-isms stems almost entirely from effects on fisheries from obviousinstances of visible disease or large mortality events. Althoughviruses infect marine organisms ranging from crustaceans to whales,we know little about modes of infection and transmission, or thereservoirs of these viruses in nature. Some of these viruses posepotential health risks to humans. For example, calici and distemperviruses are thought to cycle between marine and terrestrial mam-mals, and some marine caliciviruses are thought to cause disease inhumans82,83. Similarly, there is evidence that marine birds harbouravian flu, particularly the dangerous H5N1 strain84. We have very lit-tle understanding of the natural reservoirs of viruses that are carriedby, or cause disease in, marine animals and know even less abouttheir potential to spread to terrestrial systems. Our emerging knowl-edge of the enormous diversity of viruses in the marine milieu sug-gests that the oceans are potential reservoirs of many unknowncausative agents of disease.

oligotrophic ocean, where slow rate processes make it difficult toobtain reliable data except from visibly infected cells or viral decayrates. Moreover, the assumptions for calculating mortality rates areparticularly poorly grounded for open-ocean species. Even within rel-atively productive environments, estimates of the contribution ofviruses to total mortality range from undetectable to 100%. In manycases, the wide range in estimates is probably real, and reflects differ-ences between locations and times. Nonetheless, accurate estimates ofvirus-mediated mortality remain elusive, and we are not much furtherahead than a decade ago when viruses were estimated to kill ~20–40 %of marine bacteria on a daily basis75 and contribute to microbial mor-tality at a level similar to that of grazing by zooplankton76.

Viruses are catalysts of global nutrient cyclesGiven that viruses cause a significant, albeit variable, amount ofmarine microbial mortality, it implies that they also play an importantrole in marine geochemical cycles. Simple models4,5 and model sys-tems77 demonstrate that viruses are catalysts that accelerate the trans-formation of nutrients from particulate (living organisms) to dissolvedstates, where it can be incorporated by microbial communities (Fig. 3).A net effect of this shunt is to increase community respiration anddecrease the efficiency of carbon transfer to higher trophic levels. Inaddition, cell lysis converts particulate organic carbon (POC) into dis-solved (therefore lower levels of cellular carbon) sinks (Fig. 4), result-ing in more carbon being respired in the surface waters. This issignificant for global carbon cycling because sinking of POC results inthe net transfer of about 3 Gt of carbon between near-surface and deepwaters thus the build-up of CO2 in the atmosphere is only about half ofwhat it otherwise would be. An exception occurs in some phytoplank-

Lysis of planktonby viruses

CO2 90 Gt/y

150 Gt/y

3 Gt/y

+4 Gt/y5 Gt/y2 Gt/y

93 Gt/y

CO2

Deforestation

Biological and chemicalprocesses

DOC

POCPlankton infectedby virus

Fossil fuels

Atmosphere805 Gt

7, 000 Gt

5 Gt

700 Gt

50 Gt

Ocean38,500 Gt

Fossil fuel use

UV

ThermoclineUninfected cells anddetritus sink

Plankton

Figure 4 | Viruses can affect the efficiency of the biological pump. Viruses cause the lysis of cells, converting them into particulate organic carbon (POC) anddissolved organic carbon (DOC). This reduces the rate atwhich C sinks from the surface layer into the deep ocean where the carbon is trapped for millennia(biological pump). Instead the carbon is retained in the surface waters where it is photo-oxidized and respired, in chemical equilibrium with the atmosphere.The net effect is a faster rate of CO2 build-up in the atmosphere than would occur if the POC were ‘exported’ to the deep ocean.

04 Suttle 22-27 7/9/05 4:23 PM Page 25

Nature Publishing Group© 2005

© 2005 Nature Publishing Group

Suttle, 2005

Viral niche construction!

Case study:Baculoviridae

http://www.mardre.com/homepage/mic/tem/samples/bio/virus/bac2.htm

genera should be revised. The lepidopteranNPVs aremoreclosely related to the GVs than to the hymenopteran anddipteran NPVs (Herniou et al., 2003). Based on the rec-ommendations of the baculovirus study group (Jehle et al.,2006), the International Committee on the Taxonomy ofViruses recently approved classification of the Baculovir-idae into four genera: the Alpha, Beta, Gamma andDeltabaculoviridae.

The alphabaculoviruses include all lepidopteran NPVs,and are further divided into Group I and Group II,depending on the identity of the envelope fusion protein.Group I viruses have peplomers of GP64, whereas GroupII viruses have projections that contain baculovirus F(fusion) protein. Group I viruses also encode an F proteinhomolog, but infectivity is dependent uponGP64.Many ofthe Alphabaculoviridae are further designated as S (single)or M (multiple) phenotypes, according to the number ofnucleocapsids within the viral envelopes of occluded vir-ions. This designation was once thought to be phylo-genetically relevant, but now it is recognised that there areseveral examples of closely related S andMviruses. The useof S and M designations persists in the baculovirus litera-ture, however, because the M phenotype offers a com-parative advantage in infection (Washburn et al., 2003). Inaddition, it helps to distinguish among related viruses thatinfect the same insect. The type species of the Alphabacu-loviridae is Autographa californica nucleopolyhedrovirus(AcMNPV).

The betabaculoviruses consist of the former Granulo-virus genus. They are lepidopteran-specific viruses withocclusion-derived virus (ODV) encased in granulin. Thetype species is Cydia pomonella granulovirus (CpGV).

The genus Gammabaculoviridae includes the hymen-opteran-specific viruses. They produce occluded virus witha polyhedrin matrix, but lack GP64 or F protein. It is yetunclear whether they have orthologs that have diverged to

the point where they are unrecognisable or whether theyhave lost the genes entirely. There is some data to suggestthat the hymenopteran viruses may not spread beyond themidgut, inwhich case a budded virus (BV) formmay not benecessary (Duffy et al., 2006). The type species of theGammabaculoviridae is Neodiprion lecontei nucleopolyhe-drovirus (NeleNPV).Only onemember of the genus deltabaculovirus has been

sequenced to date.Culex nigripalpus nucleopolyhedrovirus(CuniNPV) infectsmosquitoes, amember of theDiptera. Itproduces both BV (containing F protein) and ODV. Thematrix protein shows no apparent homology to polyhedrinor granulin and may represent a new family of occlusionproteins (Perera et al., 2006).Most baculoviruses are species- or genus-specific, and

are named after the insect that they infect. A notableexception to this rule is AcMNPV, which can infect at least32 different lepidopteran insects from 12 families.

Structure

Morphology

The baculovirus life cycle involves the production of twomorphologically distinct infectious virus particles: BV andODV. Both forms consist of the viral nucleocapsid sur-rounded by an envelope. The BV envelope is acquired asvirus buds from the plasma membrane. BV envelope con-tains several viral proteins. The terminal surface pro-jections are composed of one type of a glycosylated, lowpH-activated fusion (F) protein. The Group I NPVs havepeplomers of GP64, whereas Group II NPVs, beta anddeltabaculoviruses have projections that containFprotein.BV is responsible for cell-to-cell transmission withininfected insects, and is the form used for infection in tissueculture (Figure 2). See also: Glycoproteins; Viruses:Genomes and GenomicsThe envelope of ODV is acquired in the nucleus and also

contains a number of viral proteins, some of which arecommon to BV, but the fusion protein is notably absent.The occluded virus form is required for insect-to-insecttransmission of virus. The polyhedrin or granulin matrixsurrounding ODV protects the virus from environmentaldamage during horizontal transmission. The insect hostsfor baculoviruses do not live in social groups and, there-fore, the virus cannot be spread by direct contact. Occludedvirus can persist for years when protected from ultravioletlight.The use of two viral phenotypes that are genetically

identical but morphologically distinct is an unusual andexpensive strategy for virus propagation, but itmakes sensein view of the extremely different environmental conditionswithin the gut lumen of a lepidopteran larva and in thehaemolymph (insect blood). The pH of the midgut lumenranges from 9.2 to 11.0 (depending on the species) whereashaemolymph is slightly acidic.

Virions

MNPV

SNPV

Occlusionbody

Granulovirus(GV)

Nucleopolyhedrovirus(NPV)

Figure 1 Occluded virions. Baculovirus genera are based on the structuresof occluded virus, polyhedral shaped for nucleopolyhedrovirus (NPV) withmany enveloped nucleocapsids or smaller ovoid occlusions with a singlenucleocapsid for granulovirus (GV). NPVs may contain multiplenucleocapsids (MNPV) or single nucleocapsids (SNPV).

Baculoviruses

eLS & 2011, John Wiley & Sons, Ltd. www.els.net2

Guarino, 2011

Lymantria dispar

Zombie / Gooey

Zombie / Gooeyegt chit

cath

Hoover et al, 2011Hawtin et al, 1997

How do you acquire both features?Zombie / Gooey

Zombie but not gooey?

Non-zombie, but gooey?

Susceptible Exposed Carrier Liquefied

Reservoir

�L+ �0C

µ � �

⌫ �⌧

✓

✏

R0 =⇣

�0

�+�+✓

⌘⇣⌫

⌫+µ

⌘+

⇣�

�+⌧

⌘⇣⌫

⌫+µ

⌘⇣�

�+�+✓

⌘

R0 =⇣

�0

�+�+✓

⌘⇣⌫

⌫+µ

⌘+

⇣�

�+⌧

⌘⇣⌫

⌫+µ

⌘⇣�

�+�+✓

⌘

Susceptible Exposed Carrier Liquefied

Reservoir

�L+ �0C

µ � �

⌫ �⌧

✓

✏

R0 =⇣

�0

�+�+✓

⌘⇣⌫

⌫+µ

⌘+

⇣�

�+⌧

⌘⇣⌫

⌫+µ

⌘⇣�

�+�+✓

⌘

Susceptible Exposed Carrier Liquefied

Reservoir

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µ � �

⌫ �⌧

✓

✏

R0 =⇣

�0

�+�+✓

⌘⇣⌫

⌫+µ

⌘+

⇣�

�+⌧

⌘⇣⌫

⌫+µ

⌘⇣�

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⌘

Susceptible Exposed Carrier Liquefied

Reservoir

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⌘

Susceptible Exposed Carrier Liquefied

Reservoir

�L+ �0C

µ � �

⌫ �⌧

✓

✏

R0 =⇣

�0

�+�+✓

⌘⇣⌫

⌫+µ

⌘+

⇣�

�+⌧

⌘⇣⌫

⌫+µ

⌘⇣�

�+�+✓

⌘

Susceptible Exposed Carrier Liquefied

Reservoir

�L+ �0C

µ � �

⌫ �⌧

✓

✏

R0 =⇣

�0

�+�+✓

⌘⇣⌫

⌫+µ

⌘+

⇣�

�+⌧

⌘⇣⌫

⌫+µ

⌘⇣�

�+�+✓

⌘

Susceptible Exposed Carrier Liquefied

Reservoir

�L+ �0C

µ � �

⌫ �⌧

✓

✏

� ⌧ � ✓

ZG �(1 + �) ⌧(1� �) � ✓L

Zg � ⌧ 0 ✓L

zG �(1� �) ⌧(1 + �) � ✓H

zg � ⌧ 0 ✓H

Table 3: Genotypes and their e↵ect on the model parameters.

g G

z �, ⌧, 0, ✓H �(1� �), ⌧(1 + �),�, ✓HZ �, ⌧, 0, ✓L �(1 + �), ⌧(1 + �),�, ✓H

Table 4:

tree bark, etc). Occluded NPVs in forest settings have been shown to persistas long as 41 years after a natural outbreak (Fuxa and Richter, 2001). Thus,� decreases � and reduces ⌧ in the zG genotype.

Since they do not liquefy their host (� = 0), it is assumed that the ZG

and zg phenotypes are neutral with respect to horizontal transmission of thevirus. However, the egt gene would still modify transmission to the reservoirby the same argument as above, so we can represent this by modifying thevalue of ✓. Currently, I’m just doing this by using two values, ✓H and ✓L,and setting zg to ✓H and Zg to ✓L.

I could

make this

a function

of � too,

though.Or the other way of looking at this:

4 Parameter values

I’m balancing the fact that we don’t need to tie this to any particular lepi-dopteran / baculovirus pair (largely because there’s thousands of them) withthe urge to pick parameter values that are at least vaguely realistic. So here’ssome thoughts:

The parameters that need choosing are �, �

0, µ, ⌫,�, �, ⌧, ✓, ✏. µ is the

death rate of exposed hosts, i.e. the ’natural death’ rate. � is the death rateof infectious hosts and clearance of liquefied ones. This is linked togetherbecause predators consume hosts in both states, as do conspecific cannibals.Note that the L of the model contains hosts that are dead and in the process

8

Genotypes

Zombie / Gooey

niche construction?So...

20 40 60 80 100 120 140 t0.0

0.2

0.4

0.6

0.8

1.0

Res.

Liq.

Cad.

Exp.

Sus.

Susceptible

Exposed

Cadaver

Liquefied

Reservoir

% o

f p

op

ula

tion

Time (days)

0

5

10

15

20

25

0.0 0.2 0.4 0.6 0.8γ

R0

GenotypezgzGZgZG

0

5

10

15

20

25

0.0 0.2 0.4 0.6 0.8γ

R0

GenotypezgzGZgZG

0

5

10

15

20

25

0.0 0.2 0.4 0.6 0.8γ

R0

GenotypezgzGZgZG

zg < Zg < zG < ZGFitness sequence:

=

0.1

0.2

0.3

0.4

0.5

0.5 1.0 1.5 2.0

β

θSequence

No NCZg,zG,zgzG,Zg,zgZg,zg,zGzG,zg,Zgzg,Zg,zGzg,zG,Zg

(transmission from liquefied hosts)

(reservoir contribution by carriers)

Spodoptera exigua MNPV Spodoptera litura NPV II Spodoptera frugiperda MNPV Agrotis segetum NPV Agrotis ipsilon multiple NPV Mamestra configurata NPV-A Mamestra configurata NPV-B Helicoverpa armigera multiple NPV Chrysodeixis chalcites NPV Trichoplusia ni SNPV Orgyia leucostigma NPV Euproctis pseudoconspersa NPV Ecotropis obliqua NPV Clanis bilineata NPV virus Adoxophyes honmai NPV Adoxophyes orana NPV Helicoverpa armigera NPV G4 Helicoverpa armigera NPV Helicoverpa zea SNPV Helicoverpa armigera NPV NNg1 Lymantria dispar MNPV Lymantria xylina MNPV Autographa californica NPV Rachiplusia ou MNPV Plutella xylostella multiple NPV Bombyx mori NPV Bombyx mandarina NPV Maruca vitrata MNPV Choristoneura fumiferana DEF MNPV Anticarsia gemmatalis NPV Epiphyas postvittana NPV Antheraea pernyi NPV Hyphantria cunea NPV Orgyia pseudotsugata MNPV Choristoneura fumiferana MNPV Spodoptera litura NPV Leucania separata NPV Xestia c-nigrum GV Helicoverpa armigera GV Pseudaletia unipuncta GV Spodoptera litura GV Plutella xylostella GV Agrotis segetum GV Phthorimaea operculella GV Adoxophyes orana GV Cydia pomonella GV Cryptophlebia leucotreta GV Clostera anachoreta GV Choristoneura occidentalis GV Pieris rapae GV Neodiprion sertifer NPV Neodiprion lecontii NPV Neodiprion abietis NPV Culex nigripalpus NPV

egtchitcathnull

Type I

Type II

•Infect only midgut and fat bodies.•Kill slowly, little or no liquefaction.

•Infect multiple tissues.•Kill more quickly, liquefy the host.

Granulovirus Morphs

egt chitcath

Zombie/Gooey

Xestia c-nigrum GV

Helicoverpa armigera GV

Pseudaletia unipuncta GV

Spodoptera litura GV

Plutella xylostella GV

Agrotis segetum GV

Phthorimaea operculella GV

Adoxophyes orana GV

Cydia pomonella GV

Cryptophlebia leucotreta GV

Clostera anachoreta GV

Choristoneura occidentalis GV

Pieris rapae GV

egtchitcathnull

Type IType II

niche construction!So...

Viruses are driving behaviour... for their own benefit.

Sociality?

Biopesticidesfor fun and profit!

Thanks!Tanaka Lab

Photos

Kelli Hoover, used by permission

ratsinis (Flickr) used under a CC license

GollyGForce (Flickr) used under a CC license