My talk in 2nd Finnish Molecular Ecology and Evolution Symposium, Lammi Biological Station, 13.10.2016.

1. Associations between
parasites and microbiota
in intestinal communities
of wild mammals
Tuomas Aivelo
University of Zürich
2nd Finnish Molecular Ecology Symposium
Lammi, 13.10.2016

2. • Based on hopefully very
soon (submitted)
manuscript
• Co-authored with Anna
Norberg (MRC/UH)
• Slides uploaded in
Slideshare:
Research Foundation of
University of Helsinki

3. Species interactions
in the wild
• Notoriously difficult to analyze
from observational data
• Species coexisting because of
similar habitat requirements vs.
actual interactions between
species
• But we have more and more
data...

4. Within-host interactions
• To make it even more tedious, host has both
indirect and direct influences
• Lab experiments with certain parasites (Hayes et
al., 2010; Reynolds et al., 2015)
• Perturbation experiments with only parasites
(Knowles et al, 2013; Pedersen & Fenton, 2015)
• Observational data with parasites and microbiota
(Kreising et al., 2015; Maurice et al., 2015)
• What to do with microbiota data?

5. Research Questions
• Does parasite species have
consistent association patterns with
each other or with microbiota?
• How does host variables affect the
presence of parasites or microbiota?

6. Mouse lemurs
• The smallest mammals in the world
• The cutest animals in the world
• Longitudinally tracked
• Ranomafana National Park in SE Madagascar
• Host variables: site, date, sex, age, aggression, body
condition, testis size

7. Inside mouse lemurs
• Tracked for two years for
parasites (n = 281) :
• Six species of nematodes
• Two species of cestodes
• Unicellular coccid, Eimeria
• Two ectoparasites, louse and tick
• One year for microbiota (n = 80):
• 23 OTUs collated to orders
18S metabarcoding
morphological identifications
16S metabarcoding

8. Alpha diversity: Eimeria
• Of the parasites, only Eimeria presence
associated with higher alpha diversity

9. Beta diversity
• Depending on the metrics,
cestode Hymenolepis diminuta
was associated with differences
in microbiota composition
• Jaccard: R2 = 0.015,p = 0.010
• Bray-Curtis: R2 = 0.019,p = 0.025
• Not significant with Ochiai or
Yue-Clayton
?

10. Species distribution
modelling
• Bayesian inference
• Constrained by species
traits, environmental
covariates and species
phylogeny
• Species presence-absence
as response matrix
• Based on Ovaskainen et al.
2016a, 2016b; Abrego et al.,
2016

11. Species associations

12. Which host traits are important?
• Fewer than I expected!
Eimeria
H.diminuta
H.nana
Nematode1
Nematode2
Nematode3
Nematode4
Nematode5
Nematode6
Tick
Lice
Sex/male
Age
Testis size
Body condition
Aggression
Time

13. Conclusions
• There are definite patterns of
association in the intestinal
community
• Different associations between two
Hymenolepis spp.
• Dramatic effect on diversity by
Eimeria
• Different metrics meaningful for
different parasites
• What do they actually mean?
• Eimeria vs. helminths
• Th1 vs. Th2?
• ”But you talked about
’interactions!”

14. In nutshell
Joint species modelling gives us
good hypothesis on species
interactions...
...but these need to be verified in
experimental setting...
...and we can’t still differentiate
between direct and indirect
interactions.

15. References
• Abrego, N., Dunson, D., Halme, P., Salcedo, I. & Ovaskainen, O. (2016) Wood-inhabiting fungi with tight
associations with other species have declined as a response to forest management. Oikos, (accepted).
• Hayes, K.S., Bancroft, A.J., Goldrick, M., Portsmout, C., Roberts, I.S. & Grencis, R.K. (2010) Exploitation of the
intestinal microflora by the parasitic nematode Trichuris muris. Science, 328, 1391–1395.
• Knowles, S.C.L., Fenton, A., Petchey, O.L., Jones, T.R., Barber, R. & Pedersen, A.B. (2013) Stability of within-host
– parasite communities in a wild mammal system. Proceedings of the Royal Society B: Biological Sciences, 280.
• Kreisinger, J., Bastien, G., Hauffe, H.C., Marchesi, J. & Perkins, S.E. (2015) Interactions between multiple
helminths and the gut microbiota in wild rodents. Philosophical Transactions of the Royal Society B: Biological
Sciences, 370, 20140295.
• Maurice, C.F., Cl Knowles, S., Ladau, J., Pollard, K.S., Fenton, A., Pedersen, A.B. & Turnbaugh, P.J. (2015) Marked
seasonal variation in the wild mouse gut microbiota. The ISME journal
• Ovaskainen, O., Abrego, N., Halme, P. & Dunson, D. (2016) Using latent variable models to identify large
networks of species-to-species associations at different spatial scales. Methods in Ecology and Evolution, 7,
549–555.
• Ovaskainen, O., Roy, D.B., Fox, R. & Anderson, B.J. (2016) Uncovering hidden spatial structure in species
communities with spatially explicit joint species distribution models. Methods in Ecology and Evolution, 7, 428–
436.
• Pedersen, A.B. & Fenton, A. (2015) The role of antiparasite treatment experiments in assessing the impact of
parasites on wildlife. Trends in Parasitology, 31, 200–211.
• Reynolds, L. a, Finlay, B.B. & Maizels, R.M. (2015) Cohabitation in the intestine: interactions among helminth
parasites, bacterial microbiota, and host immunity. Journal of Immunology, 195, 4059–66