Research

Virulence: when it coevolves with immunosuppression
Many components of host–parasite interactions affect the way virulence (i.e. parasite-induced harm to the host) evolves. But, theoreitcal models often ignore coevolution of multiple parasite traits. We explore how an immunosuppressive adaptation of parasites affects and coevolves with virulence in multiple infections. Using the adaptive dynamics framework to epidemiological models with coinfection, we show that immunosuppression is a double-edged sword for the evolution of virulence. On one hand, it amplifies the adaptive benefit of virulence by increasing the abundance of coinfections through epidemiological feedbacks. On the other hand, immunosuppression hinders host recovery, prolonging the duration of infection and elevating the cost of killing the host (as more opportunities for transmission will be forgone if the host dies). The balance between the cost and benefit of immunosuppression varies across different background mor- tality rates of hosts. We also find that immunosuppression evolution is influenced considerably by the precise trade-off shape determining the effect of immunosuppression on host recovery and susceptibility to further infection. These results demonstrate that the evolution of virulence is shaped by immunosuppression while highlighting that the evolution of immune evasion mechanisms deserves further research attention.

Kamiya, T., Mideo, N. and Alizon, S., 2018. Coevolution of virulence and immunosuppression in multiple infections. Journal of Evolutionary Biology, doi:10.1111/jeb.13280.

Epidemiological consequences of vector saliva
The mammalian host mounts a variety of immune responses against arthropod saliva. Experimental studies show that the immune responses elicited by previous exposure to vector saliva can alter disease severity if the host later becomes infected. This pre-sensitisation of host immunity has been linked to either exacerbation or mitigation of symptoms in a number of disease systems. We developed a general model of vector-borne disease to examine how vector control efforts alter the frequency of immune pre-sensitisation and thus change the epidemiological impact of control. We show that the abundance of pre-sensitised infected hosts should increase when control efforts moderately increase vector mortality rates. When immune pre-sensitisation leads to longer infections—by generating sub-clinical cases for which treatment is not rapidly sought—killing vectors can lead to unexpected increases in the number of infected hosts. The rising case burden may go unnoticed unless sub-clinical individuals are tested for infection. Conversely, if immune pre-sensitisation leads to more rapid clearance of infection, increasing vector mortality rates may achieve greater than expected disease control. Our findings highlight the need to quantify how immune pre-sensitisation modulates clinical outcomes and parasite transmission in humans.

Kamiya, T., Greischar, M., Mideo, N., 2017. Epidemiological consequences of immune sensitisation by pre-exposure to vector saliva. PLoS Neglected Tropical Diseases,
11(10): e0005956.

Evolution of immune systems
It's not easy to predict how much an organism should invest in defence. Induced immune defence costs little when pathogens are absent, but mounting an induced response can be time-consuming. To ensure timely protection, organisms often rely on constitutive defence even though always having one's guard up is uneconomical. Another layer of complexity is coevolutionary arms-race. If your enemy has an upper hand, is your defence really worth the cost?  My colleagues and I developed a theoretical model inspired by the invertebrate innate immune system to ask how parasite coevolution affects the optimal combination of constitutive and induced defence. Our model tells us that coevolution of parasites can shift the host’s optimal allocation from induced towards constitutive immunity. A parasite population subjected to a specific immune receptor can evolve heightened genetic diversity, which makes parasite detection more difficult for the hosts. We show that this coevolutionary feedback makes the induced immune response less efficient, forcing the hosts to invest more heavily in constitutive immunity. Our results highlight that evolutionary feedback between host and parasite populations is a key factor shaping the selection regime for immune systems.

Kamiya, T., Oña, L., Wertheim, B. and van Doorn, G.S., 2016. Coevolutionary feedback
elevates constitutive immune defence: a protein network model. BMC Evolutionary
Biology, 16(1), p.1.

Sociality in parasitic flatworms (trematodes)
Division of labour in animal societies is not limited to ants and bees. The social clonal stage of trematode parasites in snail intermediate hosts form two castes: reproductive members and non-reproductive members that are considered as soldiers. Inspired by the classic theoretical and empirical works on social insects, we investigated potential determinants of colony success in these unique clonal organisms. We found that the effect of competition from other trematode parasite species interacts with social conditions, such as caste ratio, to influence the growth of individual caste members and ultimately determine the reproductive output of those colonies. In the process, we also discovered that reproductive colony members adjust their competitive behaviour according to the number of non-reproductives in the colony, as previously seen in termite colonies.

Kamiya, T. and Poulin, R., 2013. Caste ratios affect the reproductive output of social
trematode colonies. Journal of Evolutionary Biology, 26(3), p.509-516.
Kamiya, T. and Poulin, R., 2013. Behavioural plasticity of social trematodes depends
upon social context. Biology Letters, 9(1), p.20121027.
Kamiya, T., O’Dwyer, K., Nuy, J. and Poulin, R., 2013. What determines the growth
of individual castes in social trematodes? Evolutionary Ecology, 27(6), p.1235-1247.

Biodiversity of parasites
Understanding patterns of biodiversity, and evaluating its roles in ecosystem functions are important goals for ecologists. But, parasites are often rather neglected by the mainstream biodiversity crisis debate despite their richness and functional importance to ecosystems and evolutionary processes. Using meta-analytic techniques, we explored major determinants of parasite species richness.

Kamiya, T., O’Dwyer, K., Nakagawa, S. and Poulin, R., 2014. Host diversity drives
parasite diversity: meta–analytical insights into patterns and causal mechanisms.
Ecography, 37(7), p.689-697.
Kamiya, T. , O’Dwyer, K., Nakagawa, S. and Poulin, R., 2014. What determines
species richness of parasitic organisms? A meta–analysis across animal, plant and
fungal hosts. Biological Reviews, 89(1), p.123-134.

Parasite-induced behavioural alteration
Parasites are known to alter behaviours of their hosts through pathogenic side effects or sometimes in order to adaptively improve their chance of transmission to the next host. I investigate how trematode infection affects the trade-off between foraging and predator evasion in a marine snail. I found that some species of parasites make their host less sensitive to predator odours, leaving the snail host more vulnerable to crab predators.
    We have also looked into how trematode parasites affect the use of microhabitat of their rockyshore snail hosts. Through a mark-recapture study, we found that infected snails spend more time on the rocky surface instead of in crevice; this altered behaviour is likely to make the snails more vulnerable to predation by birds which serve as the definitive hosts for the trematode.

O’Dwyer, K., Kamiya, T. and Poulin, R., 2014. Altered microhabitat use and movement of littorinid gastropods: the effects of parasites. Marine Biology, 161(2), p.437-445.
Kamiya, T. and Poulin, R., 2012. Parasite–induced behavioural changes to the trade–off between foraging and predator evasion in a marine snail. Journal of Experimental Marine Biology and Ecology, 438, p.61-67.