Assemblage dynamics and evolution of pathogen communities

Benjamin Roche

What do we want to understand with community ecology? •

How does the biodiversity dynamics work? •

Why do species coexist or not?



Why some species are more abundant than others?

Structure of communities •

Vertebrates follow a lognormal distribution Preston 1948



Invertebrates follow a geometric distribution Fisher 1943

What could explain these structures?

Niche theory

Neutral theory

Environmental factor 2

What is a niche organism? Fondamental niche

Fundamental niche: « space » occupied by the organism in absence of competitors

Realized niche

Environmental factor 1

Realized niche: « space » occupied by the organism in presence of competitors

What is a niche organism? Principle of Mutually competitive exclusion: Realized niches of two organisms cannot overlap Niche organism is « unique » Resource Community structure is driven by local interactions between species

Neutral theory

Neutral theory

Community structure is driven by species dispersal between local communities Hubbell 2001

Some consensual views?

Pathogens also interact

Pathogen interactions

Pathogen interactions

60 pt 60 pt

Interactions through immune system: the case of Plasmodium falciparum and helminths Th2

Th1 Th1

Interactions through immune system: the case of Plasmodium falciparum and helminths

Percentage

100%

0% Non malaria

TNF α (pg/ml)

Mild malaria

>250

50-250

Adapted from Kwiatkowski et al., Lancet 1990, 1201-1204

Cerebral malaria

10-50

Cerebral Malaria (deaths)

<10

Pathogen interactions

Interactions within populations

Illustration: John Megahan

Interactions within populations: measles and pertussis

Cases

measles Epidemics every two years

Time

Cases

pertussis Epidemics every 4 years Time

Similar transmissibility (R0 ~17)

Interactions within populations: measles and pertussis

Cases

measles Epidemics every two years

Time

Cases

pertussis Epidemics Epidemics every every24years years Time

Similar transmissibility (R0 ~17)

Interactions within populations

Rohani et al, Proc Roy Soc B,1998

Interactions within populations

Temps

Temps Rohani et al, Nature, 2001

Pathogen interactions

Inter-specific interactions

Pathogen interactions

The influenza story •

RNA viruses with high mutation rate



Large diversity, classified into subtypes



Infect a lot of species, especially wild birds

Cross-immunity process

Amino acid differences

Adapted from Park et al, Science, 2009

Amino acid differences

Cross-immunity process: consequences

Mac Hardy and Adams, PLoS Pathogens, 2009

The avian influenza story

The observation •

Different coexistence patterns



Restricted subtype diversity in humans •



A lot of research has addressed the reason of that

Large subtype diversity in wild birds •

No clear consensus…

A possible explanation •

Existence of an environmental transmission in wild birds suggested by higher prevalence in aquatic birds



Experimental evidence that viral particles can persist during a long time in aquatic environment

Brown et al, IGE, 2009

Epidemiological evidence Roche et al, IGE, 2009

Going down in the scale…

Statistical approach to identify the main contributors •

Multiple regression analysis with elastic-net regression



Explaining statistically the genetic diversity of each subtype according to: •

Persistence value



Host diversity



Spatial configuration



Sequence characteristics

Relative contribution of each component Hypothesis

Estimation

Coefficient

Nucleotide mutation rate

0.27

Shannon index

0.11

Geographic structuring

Fst

-0.28

Host immunity

Amino acid substitution rate

-0.995

Experimental measure

0.68

Mutation rate Host diversity

Environmental durability Roche et al, PLoS Biology, 2014

Exploring the impact of environmental transmission •

Developing an individualbased model to consider multiple strains configuration



Possibility to infer digital phylogeny

Roche et al, BMC Bioinformatics, 2010

Model outcomes

Roche et al, PLoS Biology, 2014

Contribution of environmental persistence •

Environmental persistence is needed to have a high genetic diversity



But short lifespan is also required

Roche et al, PLoS Biology, 2014

The hypothesis

A test of the hypothesis •

Each subtype has a different environmental durability



Genetic diversity of AIV is correlated with persistance duration

The source of pandemic flu •

Sometimes, one influenza strain yields to pandemics



The most famous one is the Spanish flu, that kills between 20 and 40 millions of people at the end of WWI



Caused by a large antigenic shift (rather than an antigenic drift)

The avian influenza story

Pathogens form community

Defining pathogen’s niche

Roche et al, 2014, BMC Public Health

Defining pathogen’s niche

Roche et al, 2014, BMC Public Health

Pathogen community

Guernier et al, PLoS Biology, 2003

Pathogen’s niche

Pathogen’s interactions: an issue for public health?

Understanding pathogen biodiversity •

Community structure of large organisms is still not entirely understood



This is similar for (micro-)parasites (in humans)



Pathogen community structure is probably driven at large (global) and very localized (within-host) scales



Such pathogen interactions have to be considered for public health and veterinary concerns

Assemblage dynamics and evolution of pathogen communities

Benjamin Roche

Benjamin Roche

transmission in wild birds suggested by higher prevalence in ... environmental transmission. • Developing an individual- ... the end of WWI. • Caused by a large ...

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