Romain Garnier

Maternal antibody persistence: a neglected life-history trait with implications from albatross conservation to comparative immunology

The evolution of different life-history strategies has been suggested as a major force constraining physiological mechanisms such as immunity. In some long-lived oviparous species, a prolonged persistence of maternal antibodies in offspring could thus be expected in order to protect them over their long growth period. Here, using an intergenerational vaccination design, we show that specific maternal antibodies can display an estimated half-life of 25 days post-hatching in the nestlings of a long-lived bird. This temporal persistence is much longer than previously known for birds and it suggests specific properties in the regulation of IgY immunoglobulin catabolism in such a species. We also show that maternal antibodies in the considered procellariiform species are functional as late as 20 days of age. Using a modelling approach, we highlight that the potential impact of such effects on population viability could be important, notably when using vaccination for conservation. These results have broad implications, from comparative immunology to evolutionary eco-epidemiology and conservation biology.

Coevolution between maternal transfer of immunity and other resistance strategies against pathogens.

Among the wide variety of resistance mechanisms to parasitism, the transgenerational transfer of immunity from mother to offspring has largely been overlooked and never included in evolutionary or coevolutionary studies of resistance mechanisms. Here we study the evolution and coevolution of various resistance mechanisms with a special focus on maternal transfer of immunity. In particular we show that maternal transfer of immunity is only expected to evolve when cross immunity is high and when the pathogens have an intermediate virulence. We also show that the outcome of the coevolution between various resistance mechanisms depends critically on the life span of the host. We predict that short‐lived species should invest in avoidance strategies, whereas long‐lived species should invest in acquired resistance mechanisms. These results may help understanding the diversity of resistance strategies that have evolved in vertebrate species. Our framework also provides a general basis for the study of the evolution of other transgenerational resistance mechanisms.

Heritable, Heterogeneous, and Costly Resistance of Sheep against Nematodes and Potential Feedbacks to Epidemiological Dynamics*

Infected hosts may preserve fitness by resisting parasites (reducing parasite burden) and/or tolerating them (preventing or repairing infection-induced damage). Theory predicts that these individual-level defense strategies generate divergent population-level feedbacks that would maintain genetic heterogeneity for resistance but purge heterogeneity for tolerance. Because resistance reduces parasite abundance, selection for costly resistance traits will weaken as resistance becomes common. Such negative frequency-dependent selection contrasts with predictions for tolerance, which maintains parasite abundance and so is expected to generate positive frequency-dependent selection, unless, for example, tolerance trades off with resistance. Thus far, there have been few tests of this theory in natural systems. Here, we begin testing the predictions in a mammalian field system, using data on individual gastrointestinal nematode burdens, nematode-specific antibody titers (as a resistance metric), the slope of body weight on parasite burden (as a tolerance metric), and fitness from an unmanaged population of Soay sheep. We find that nematode resistance is costly to fitness and underpinned by genetic heterogeneity, and that resistance is independent of tolerance. Drawing upon empirical metrics such as developed here, future work will elucidate how resistance and tolerance feedbacks interact to generate population-scale patterns in the Soay sheep and other field systems.

Evolution of transgenerational immunity in invertebrates

Over a decade ago, the discovery of transgenerational immunity in invertebrates shifted existing paradigms on the lack of sophistication of their immune system. Nonetheless, the prevalence of this trait and the ecological factors driving its evolution in invertebrates remain poorly understood. Here, we develop a theoretical host–parasite model and predict that long lifespan and low dispersal should promote the evolution of transgenerational immunity. We also predict that in species that produce both philopatric and dispersing individuals, it may pay to have a plastic allocation strategy with a higher transgenerational immunity investment in philopatric offspring because they are more likely to encounter locally adapted pathogens. We review all experimental studies published to date, comprising 21 invertebrate species in nine different orders, and we show that, as expected, longevity and dispersal correlate with the transfer of immunity to offspring. The validity of our prediction regarding the plasticity of investment in transgenerational immunity remains to be tested in invertebrates, but also in vertebrate species. We discuss the implications of our work for the study of the evolution of immunity, and we suggest further avenues of research to expand our knowledge of the impact of transgenerational immune protection in host–parasite interactions.

Migration, Prospecting, Dispersal? What Host Movement Matters for Infectious Agent Circulation?

Spatial disease ecology is emerging as a new field that requires the integration of complementary approaches to address how the distribution and movements of hosts and parasites may condition the dynamics of their interactions. In this context, migration, the seasonal movement of animals to different zones of their distribution, is assumed to play a key role in the broad scale circulation of parasites and pathogens. Nevertheless, migration is not the only type of host movement that can influence the spatial ecology, evolution, and epidemiology of infectious diseases. Dispersal, the movement of individuals between the location where they were born or bred to a location where they breed, has attracted attention as another important type of movement for the spatial dynamics of infectious diseases. Host dispersal has notably been identified as a key factor for the evolution of host-parasite interactions as it implies gene flow among local host populations and thus can alter patterns of coevolution with infectious agents across spatial scales. However, not all movements between host populations lead to dispersal per se. One type of host movement that has been neglected, but that may also play a role in parasite spread is prospecting, i.e., movements targeted at selecting and securing new habitat for future breeding. Prospecting movements, which have been studied in detail in certain social species, could result in the dispersal of infectious agents among different host populations without necessarily involving host dispersal. In this article, we outline how these various types of host movements might influence the circulation of infectious disease agents and discuss methodological approaches that could be used to assess their importance. We specifically focus on examples from work on colonial seabirds, ticks, and tick-borne infectious agents. These are convenient biological models because they are strongly spatially structured and involve relatively simple communities of interacting species. Overall, this review emphasizes that explicit consideration of the behavioral and population ecology of hosts and parasites is required to disentangle the relative roles of different types of movement for the spread of infectious diseases.

Long Antibody Persistence and Transgenerational Transfer of Immunity in a Long-Lived Vertebrate

Although little studied in natural populations, the persistence of immunoglobulins may dramatically affect the dynamics of immunity and the ecology and evolution of host-pathogen interactions involving vertebrate hosts. By means of a multiple-year vaccination design against Newcastle disease virus, we experimentally addressed whether levels of specific antibodies can persist over several years in females of a long-lived procellariiform seabird—Cory’s shearwater—and whether maternal antibodies against that antigen could persist over a long period in offspring several years after the mother was exposed. We found that a single vaccination led to high levels of antibodies for several years and that the females transmitted antibodies to their offspring that persisted for several weeks after hatching even 5 years after a single vaccination. The temporal persistence of maternally transferred antibodies in nestlings was highly dependent on the level at hatching. A second vaccination boosted efficiently the level of antibodies in females and thus their transfer to offspring. Overall, these results stress the need to consider the temporal dynamics of immune responses if we are to understand the evolutionary ecology of host-parasite interactions and trade-offs between immunity and other life-history characteristics, in particular in long-lived species. They also have strong implications for conservation when vaccination may be used in natural populations facing disease threats.

Insights from Parasite-Specific Serological Tools in Eco-Immunology

Abstract Eco-immunology seeks evolutionary explanations for the tremendous variation in immune defense observed in nature. Assays to quantify immune phenotypes often are crucial to this endeavor. To this end, we suggest that more use could (and arguably should) be made of the veterinary and clinical serological toolbox. For example, measuring the magnitude and half-life of parasite-specific antibodies across a range of host taxa may provide new ways of testing theories in eco-immunology. Here, we suggest that antibody assays developed in veterinary and clinical immunology and epidemiology provide excellent tools—or at least excellent starting points for development of tools—for tests of such hypotheses. We review how such assays work and how they may be optimized for new questions and new systems in eco-immunology. We provide examples of the application of such tools to eco-immunological studies of seabirds and mammals, and suggest a decision-tree to aid development of assays. We expect that addition of such tools to the eco-immunological toolbox will promote progress in the field and help elucidate how immune systems function and why they vary in nature.

Evolution of the temporal persistence of immune protection

The evolution of resistance to parasites has been the focus of numerous theoretical studies and several mechanisms, ranging from innate to acquired immune responses, have been considered. Life-history theory predicts that long-lived species should invest more resources into maintenance and immunity than short-lived species. Here, we provide further theoretical and empirical support for this hypothesis. First, an analysis of the evolution of the persistence of immune protection in a theoretical framework accounting for maternal transfer of immunity reveals that longer-lived hosts are expected to invest in more persistent intragenerational and transgenerational immune responses. Controlling for phylogenetic structure and for the confounding effect of catabolic activity, we further showed that immunoglobulin half-life and longevity are positively correlated in mammal species. Our study confirms that persistence of immunity has evolved as part of elaborate anti-parasitic defence strategies.

Length of intervals between epidemics: evaluating the influence of maternal transfer of immunity.

The length of intervals between epidemic outbreaks of infectious diseases is critical in epidemiology. In several species of marine mammals and birds, it is pivotal to also consider the life history of the species of concern, as the contact rate between individuals can have a seasonal flux, for example, due to aggregations during the breeding season. Recently, particular interest has been given to the role of the dynamics of immunity in determining the intervals between epidemics in wild animal populations. One potentially powerful, but often neglected, process in this context is the maternal transfer of immunity. Here, we explore theoretically how the transfer of maternal antibodies can delay the recurrence of epidemics using Phocine Distemper in harbor seals as an example of a system in which epidemic outbreaks are followed by pathogen extinction. We show that the presence of temporarily protected newborns can significantly increase the predicted interval between epidemics, and this effect is strongly dependent on the degree of synchrony in the breeding season. Furthermore, we found that stochasticity in the onset of epidemics in combination with maternally acquired immunity increases the predicted intervals between epidemics even more. These effects arise because newborns with maternal antibodies temporarily boost population level immunity above the threshold of herd immunity, particularly when breeding is synchronous. Overall, our results show that maternal antibodies can have a profound influence on the dynamics of wildlife epidemics, notably in gregarious species such as many marine mammals and seabirds.

Joint associations of blood plasma proteins with overwinter survival of a large mammal

In many wild animal populations, hosts are at risk of parasites and malnutrition and resource costs of defence may be difficult to afford. We postulate that proteins, important in homeostasis and immunity, play a complex but central role in condition dependence and resource costs of mammalian immune defence. To test this, we measured plasma concentrations of albumin, total proteins. Self-reactive antibodies and parasite-specific IgG in female Soay sheep. Using a principal component analysis, we found a new metric of condition reflecting individual variation in acquisition, assimilation and/or recycling of plasma proteins that predicted overwinter survival. Controlling for this metric, an age-dependent trade-off between antibody titres and protein reserves emerged, indicating costs of mounting an antibody response: younger individuals survived best when prioritising immunity while older individuals fared better when maintaining high-protein nutritional plane. These findings suggest fascinating roles for protein acquisition and allocation in influencing survival in wild animal populations.