Thierry Boulinier

Food availability affects the maternal transfer of androgens and antibodies into eggs of a colonial seabird

Mothers can improve the quality of their offspring by increasing the level of certain components in their eggs. To examine whether or not mothers increase deposition of such components in eggs as a function of food availability, we food‐supplemented black‐legged kittiwake females (Rissa tridactyla) before and during egg laying and compared deposition of androgens and antibodies into eggs of first and experimentally induced replacement clutches. Food‐supplemented females transferred lower amounts of androgens and antibodies into eggs of induced replacement clutches than did non‐food‐supplemented mothers, whereas first clutches presented no differences between treatments. Our results suggest that when females are in lower condition, they transfer more androgens and antibodies into eggs to facilitate chick development despite potential long‐term costs for juveniles. Females in prime condition may avoid these potential long‐term costs because they can provide their chicks with more and higher quality resources.

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.

Laridae: A neglected reservoir that could play a major role in avian influenza virus epidemiological dynamics

Abstract Avian influenza viruses (AIVs) are of great concern worldwide due to their economic impact and the threat they represent to human health. As wild birds are the natural reservoirs of AIVs, understanding AIV dynamics in different avian taxa is essential for deciphering the epidemiological links between wildlife, poultry and humans. To date, only the Anatidae (ducks, geese and swans) have been widely studied. Here, we aim to shed light on the current state of knowledge on AIVs in Laridae (gulls, terns and kittiwakes) versus that in Anatidae by setting forth four fundamental questions: how, when, where and to which host species are AIVs transmitted? First, we describe ecological differences between Laridae and Anatidae and discuss how they may explain observed contrasts in preferential transmission routes and the evolution of specific AIV subtypes. Second, we highlight the dissimilarities in the temporal patterns of AIV shedding between Laridae and Anatidae and address the role that immunity likely plays in shaping these patterns. Third, we underscore that Laridae may be key in promoting intercontinental exchanges of AIVs. Finally, we emphasize the crucial epidemiological position that Laridae occupy between wildlife, domestic birds and humans.

Circulation of a Meaban-like virus in yellow-legged gulls and seabird ticks in the western Mediterranean basin.

In recent years, a number of zoonotic flaviviruses have emerged worldwide, and wild birds serve as their major reservoirs. Epidemiological surveys of bird populations at various geographical scales can clarify key aspects of the eco-epidemiology of these viruses. In this study, we aimed at exploring the presence of flaviviruses in the western Mediterranean by sampling breeding populations of the yellow-legged gull (Larus michahellis), a widely distributed, anthropophilic, and abundant seabird species. For 3 years, we sampled eggs from 19 breeding colonies in Spain, France, Algeria, and Tunisia. First, ELISAs were used to determine if the eggs contained antibodies against flaviviruses. Second, neutralization assays were used to identify the specific flaviviruses present. Finally, for colonies in which ELISA-positive eggs had been found, chick serum samples and potential vectors, culicid mosquitoes and soft ticks (Ornithodoros maritimus), were collected and analyzed using serology and PCR, respectively. The prevalence of flavivirus-specific antibodies in eggs was highly spatially heterogeneous. In northeastern Spain, on the Medes Islands and in the nearby village of LEscala, 56% of eggs had antibodies against the flavivirus envelope protein, but were negative for neutralizing antibodies against three common flaviviruses: West Nile, Usutu, and tick-borne encephalitis viruses. Furthermore, little evidence of past flavivirus exposure was obtained for the other colonies. A subset of the Ornithodoros ticks from Medes screened for flaviviral RNA tested positive for a virus whose NS5 gene was 95% similar to that of Meaban virus, a flavivirus previously isolated from ticks of Larus argentatus in western France. All ELISA-positive samples subsequently tested positive for Meaban virus neutralizing antibodies. This study shows that gulls in the western Mediterranean Basin are exposed to a tick-borne Meaban-like virus, which underscores the need of exploring the spatial and temporal distribution of this flavivirus as well as its potential pathogenicity for animals and humans.

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.

Estimating transitions between states using measurements with imperfect detection: application to serological data.

Classifying the states of an individual and quantifying transitions between states are crucial while modeling animal behavior, movement, and physiologic status. When these states are hidden or imperfectly known, it is particularly convenient to relate them to appropriate quantitative measurements taken on the individual. This task is, however, challenging when quantitative measurements are not available at each sampling occasion. For capture-recapture data, various ways of incorporating such non-discrete information have been used, but they are either ad hoc and/or use a fraction of the available information by relying on a priori thresholds to assign individual states. Here we propose assigning discrete states based on a continuous measurement, and then modeled survival and transition probabilities based on these assignments. The main advantage of this new approach is that a more informative use of the non-discrete information is done. As an illustrative working example, we applied this approach to eco-epidemiological data collected across a series of years in which individuals of a long-lived seabird, the Black-legged Kittiwake (Rissa tridactyla), could either be visually detected or physically recaptured and blood sampled for subsequent immunological analyses. We discuss how this approach opens many perspectives in eco-epidemiology, but also more broadly, in population ecology.

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.

The role of seabirds of the Iles Eparses as reservoirs and disseminators of parasites and pathogens

n Abstractn n The role of birds as reservoirs and disseminators of parasites and pathogens has received much attention over the past several years due to their high vagility. Seabirds are particularly interesting hosts in this respect. In addition to incredible long-distance movements during migration, foraging and prospecting, these birds are long-lived, site faithful and breed in dense aggregations in specific colony locations. These different characteristics can favor both the local maintenance and large-scale dissemination of parasites and pathogens. The Iles Eparses provide breeding and feeding grounds for more than 3 million breeding pairs of seabirds including at least 13 species. Breeding colonies on these islands are relatively undisturbed by human activities and represent natural metapopulations in which seabird population dynamics, movement and dispersal can be studied in relation to that of circulating parasites and pathogens. In this review, we summarize previous knowledge and recently-acquired data on the parasites and pathogens found in association with seabirds of the Iles Eparses. These studies have revealed the presence of a rich diversity of infectious agents (viruses, bacteria and parasites) carried by the birds and/or their local ectoparasites (ticks and louse flies). Many of these agents are widespread and found in other ecosystems confirming a role for seabirds in their large scale dissemination and maintenance. The heterogeneous distribution of parasites and infectious agents among islands and seabird species suggests that relatively independent metacommunities of interacting species may exist within the western Indian Ocean. In this context, we discuss how the patterns and determinants of seabird movements may alter parasite and pathogen circulation. We conclude by outlining key aspects for future research given the baseline data now available and current concerns in eco-epidemiology and biodiversity conservation.n n

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.