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Optimal immune specificity at the intersection of host life history and parasite epidemiology.

ABSTRACT: Hosts diverge widely in how, and how well, they defend themselves against infection and immunopathology. Why are hosts so heterogeneous? Both epidemiology and life history are commonly hypothesized to influence host immune strategy, but the relationship between immune strategy and each factor has commonly been investigated in isolation. Here, we show that interactions between life history and epidemiology are crucial for determining optimal immune specificity and sensitivity. We propose a demographically-structured population dynamics model, in which we explore sensitivity and specificity of immune responses when epidemiological risks vary with age. We find that variation in life history traits associated with both reproduction and longevity alters optimal immune strategies-but the magnitude and sometimes even direction of these effects depends on how epidemiological risks vary across life. An especially compelling example that explains previously-puzzling empirical observations is that depending on whether infection risk declines or rises at reproductive maturity, later reproductive maturity can select for either greater or lower immune specificity, potentially illustrating why studies of lifespan and immune variation across taxa have been inconclusive. Thus, the sign of selection on the life history-immune specificity relationship can be reversed in different epidemiological contexts. Drawing on published life history data from a variety of chordate taxa, we generate testable predictions for this facet of the optimal immune strategy. Our results shed light on the causes of the heterogeneity found in immune defenses both within and among species and the ultimate variability of the relationship between life history and immune specificity.

SUBMITTER: Downie AE

PROVIDER: S-EPMC8730424 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:There is growing interest in the role that life-history traits of hosts, such as their 'pace-of-life', play in the evolution of resistance and tolerance to parasites. Theory suggests that, relative to host species that have high syntopy (local spatial and temporal overlap) with parasites, host species with low syntopy should have lower selection pressures for more constitutive (always present) and costly defences, such as tolerance, and greater reliance on more inducible and cheaper defences, such as behaviour. Consequently, we postulated that the degree of host-parasite syntopy, which is negatively correlated with host pace-of-life (an axis reflecting the developmental rate of tadpoles and the inverse of their size at metamorphosis) in our tadpole-parasitic cercarial (trematode) system, would be a negative and positive predictor of behavioural resistance and tolerance, respectively. To test these hypotheses, we exposed seven tadpole species to a range of parasite (cercarial) doses crossed with anaesthesia treatments that controlled for anti-parasite behaviour. We quantified host behaviour, successful and unsuccessful infections, and each species' reaction norm for behavioural resistance and tolerance, defined as the slope between cercarial exposure (or attempted infections) and anti-cercarial behaviours and mass change, respectively. Hence, tolerance is capturing any cost of parasite exposure. As hypothesized, tadpole pace-of-life was a significant positive predictor of behavioural resistance and negative predictor of tolerance, a result that is consistent with a trade-off between behavioural resistance and tolerance across species that warrants further investigation. Moreover, these results were robust to considerations of phylogeny, all possible re-orderings of the three fastest or slowest paced species, and various measurements of tolerance. These results suggest that host pace-of-life and host-parasite syntopy are powerful drivers of both the strength and type of host defence strategies against parasites. Future research should evaluate how often and how strongly host pace-of-life and host-parasite syntopy are correlated and which is the better predictor of the strength and type of host investments in anti-parasite defences.

Project description:BACKGROUND:Adults and larvae of generalist parasites are exposed to diverse hosts and local environmental conditions throughout their life cycles, thus local adaptation is expected to occur through phenotypic plasticity and/or natural selection. We investigated how the combined effect of cryptic host specificity and local selective pressures could shape reproductive traits of a putative generalist parasite in the oceanic realm. METHODS:The LSU rDNA, ITS2 and the mt-COI of individuals of the digenean Pholeter gastrophilus (Kossack, 1910) Odhner, 1914 (Heterophyidae Leiper, 1909) from oceanic striped dolphins, Stenella coeruleoalba Meyen, and coastal bottlenose dolphins, Tursiops truncatus Montagu, in the western Mediterranean were used to elucidate whether worms were conspecific. Infection parameters were compared between both dolphin species. General Linear Mixed Models were used to analyse the influence of host species on four reproductive traits of P. gastrophilus: body size, maturity stage (non-gravid/gravid), egg size, and number of eggs in utero. AIC values were used to rank competing models, and p-values to assess the effect of specific predictors. RESULTS:Evidence indicated that worms collected from both dolphin species were conspecific. All worms collected were gravid and infection parameters did not differ between dolphin species. However, body size and egg size of individuals of P. gastrophilus were significantly larger in striped dolphins. The number of eggs in utero did not significantly differ between dolphin species but, for a given body size, worms in bottlenose dolphins harboured more eggs. A trade-off between egg size and egg number was found in worms from both dolphin species, with a higher slope in striped dolphins. CONCLUSIONS:Apparently, striped dolphin is a more suitable host for P. gastrophilus, but reproductive investment seems to be adapted to the habitat where the life-cycle develops. Worms from striped dolphins likely face the problem of finding intermediate hosts in the oceanic realm and apparently invest into offspring size to enhance the early survival of larvae and the potential to multiply asexually within the first intermediate host. The small-sized worms from bottlenose dolphins would be adapted to reproduce early because of higher adult mortality, generating smaller and numerous eggs in a coastal habitat where chances of transmission are presumably higher.

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Optimal immune specificity at the intersection of host life history and parasite epidemiology.

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