Abstract
Seasonal disease and parasitic infection are common across organisms, including humans, and there is increasing evidence for intrinsic seasonal variation in immune systems. Changes are orchestrated through organisms' physiological clocks using cues such as day length. Ample research in diverse taxa has demonstrated multiple immune responses are modulated by photoperiod, but to date, there have been few experimental demonstrations that photoperiod cues alter susceptibility to infection. We investigated the interactions among photoperiod history, immunity and susceptibility in laboratory-bred three-spined stickleback (a long-day breeding fish) and its external, directly reproducing monogenean parasite Gyrodactylus gasterostei. We demonstrate that previous exposure to long-day photoperiods (PLD) increases susceptibility to infection relative to previous exposure to short days (PSD), and modifies the response to infection for the mucin gene muc2 and Treg cytokine foxp3a in skin tissues in an intermediate 12 L : 12 D photoperiod experimental trial. Expression of skin muc2 is reduced in PLD fish, and negatively associated with parasite abundance. We also observe inflammatory gene expression variation associated with natural inter-population variation in resistance, but find that photoperiod modulation of susceptibility is consistent across host populations. Thus, photoperiod modulation of the response to infection is important for host susceptibility, highlighting new mechanisms affecting seasonality of host–parasite interactions.
Highlights
Seasonality, whether hot–cold or wet–dry, is a prominent, ubiquitous and predictable environmental fluctuation necessitating substantial organismal plasticity
RES fish showed little difference in parasite abundance between PLD and previous exposure to short days (PSD) groups. These results suggest that PLD photoperiod treatments increased susceptibility in all fish; in RES fish, the effect is driven by PSD fish clearing their infections rather than having lower abundances
We have experimentally confirmed a causal link between photoperiod and host susceptibility to a naturally occurring parasite in a controlled setting
Summary
Seasonality, whether hot–cold or wet–dry, is a prominent, ubiquitous and predictable environmental fluctuation necessitating substantial organismal plasticity. Relative resource limitation in winter restricts many physiological processes including immune responses; behavioural changes among hosts, such as aggregating while breeding, can affect transmission of parasites and pathogens among hosts [3]; and seasonal synchronization of development times [4] or increases in the abundance of a parasite or its vectors [5,6] modulates infection risk. May be less significant for other seasonal physiological changes, such as reproduction, in non-mammals [6], but probably plays important roles in immune-mediation in fish [21]. We housed fish in contrasting photoperiods to induce changes in fish physiology, including immune responses, before conducting a controlled, factorial infection experiment with live parasites to examine the interplay between day length, natural resistance and susceptibility to a naturally occurring parasite. We expected a stronger effect of day length in hosts bred from our naturally resistant population
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