Stéphane Cornet

Patterns of aging in the long-lived wandering albatross

How does an animal age in natural conditions? Given the multifaceted nature of senescence, identifying the effects of age on physiology and behavior remains challenging. We investigated the effects of age on a broad array of phenotypic traits in a wild, long-lived animal, the wandering albatross. We studied foraging behavior using satellite tracking and activity loggers in males and females (age 6–48+ years), and monitored reproductive performance and nine markers of baseline physiology known to reflect senescence in vertebrates (humoral immunity, oxidative stress, antioxidant defenses, and hormone levels). Age strongly affected foraging behavior and reproductive performance, but not baseline physiology. Consistent with results of mammal and human studies, age affected males and females differently. Overall, our findings demonstrate that age, sex, and foraging ability interact in shaping aging patterns in natural conditions. Specifically, we found an unexpected pattern of spatial segregation by age; old males foraged in remote Antarctica waters, whereas young and middle-aged males never foraged south of the Polar Front. Old males traveled a greater distance but were less active at the sea surface, and returned from sea with elevated levels of stress hormone (corticosterone), mirroring a low foraging efficiency. In contrast to findings in captive animals and short-lived birds, and consistent with disposable soma theory, we found no detectable age-related deterioration of baseline physiology in albatrosses. We propose that foraging efficiency (i.e., the ability of individuals to extract energy from their environment) might play a central role in shaping aging patterns in natural conditions.

Variation in immune defence among populations of Gammarus pulex (Crustacea: Amphipoda)

Despite intensive studies in ecological immunology, few have investigated variation in immune defence among natural populations; in particular, there is a lack of knowledge of the sources of spatial variability in immune defence in the wild. Here we documented variation among twelve populations of the freshwater crustacean Gammarus pulex in the activity of the prophenoloxidase (ProPO) system, which is an important component of invertebrate immunity. We then tested for trade-offs between investment in immune defence and fitness-related traits such as survival and fecundity, as well as for environmental causes of variability (water temperature and conductivity, parasite prevalence). Levels of immune defence differed among populations, with environment partly explaining this population effect, as immune activities were negatively related to water conductivity and acanthocephalan parasite prevalence. There was a strong variation among populations for the maintenance of the ProPO system, while variation in its use was relatively weak. Such a pattern could be partly explained by the relative costs associated with the maintenance and/or the use of the ProPO system. Investment in the ProPO system was negatively correlated to survival, whereas it was positively related to female fecundity and resource storage. However, variation in immunity did not predict resistance to bacterial infection among populations, suggesting that measuring the activity of the ProPO system might not be sufficient to estimate immunocompetence at the population level. These results suggest that investment in immune function is a variable trait, which might be locally optimized as a result of both life history trade-offs and environmental conditions, highlighting the need to combine them in a common framework.

Immune depression induced by acanthocephalan parasites in their intermediate crustacean host: Consequences for the risk of super-infection and links with host behavioural manipulation

Parasite survival in hosts mainly depends on the capacity to circumvent the host immune response. Acanthocephalan infections in gammarids are linked with decreased activity of the prophenoloxidase (ProPO) system, suggesting an active immunosuppression process. Nevertheless, experimental evidence for this hypothesis is lacking: whether these parasites affect several immune pathways is unknown and the consequences of such immune change have not been investigated. In particular, the consequences for other pathogens are not known; neither are the links with other parasite-induced manipulations of the host. Firstly, using experimental infections of Pomphorhynchus laevis we confirmed that the lower immune activity in parasitised Gammarus pulex is induced by the parasite infection. Second, using natural infections of three different parasites, P. laevis, Pomphorhynchus tereticollis and Polymorphus minutus, we showed that acanthocephalan infection was associated with reduction of the activity of the ProPO system and the haemocyte concentration (two major parameters of crustacean immunity) suggesting that immune depression is a phenomenon affecting several immunological activities. This was confirmed by the fact that acanthocephalan infection (whatever the parasite species) was linked to a lower efficiency to eliminate a bacterial infection. The result suggests a cost of parasite immune depression. Finally, acanthocephalans are also known to induce behavioural alterations in the intermediate host which favour their transmission to definitive hosts. We did not find any correlation between behavioural and immunological alterations in both experimentally and naturally-infected gammarids. Overall, this study suggests that whilst immune depression might be beneficial to acanthocephalan survival within the intermediate gammarid host, it might also be costly if it increases host mortality to additional infections before transmission of the parasite.

Is there a role for antioxidant carotenoids in limiting self-harming immune response in invertebrates?

Innate immunity relies on effectors, which produce cytotoxic molecules that have not only the advantage of killing pathogens but also the disadvantage of harming host tissues and organs. Although the role of dietary antioxidants in invertebrate immunity is still unknown, it has been shown in vertebrates that carotenoids scavenge cytotoxic radicals generated during the immune response. Carotenoids may consequently decrease the self-harming cost of immunity. A positive relationship between the levels of innate immune defence and circulating carotenoid might therefore be expected. Consistent with this hypothesis, we show that the maintenance and use of the prophenoloxidase system strongly correlate with carotenoid concentration in haemolymph within and among natural populations of the crustacean Gammarus pulex.

Sperm depletion, male mating behaviour and reproductive ‘time-out’ in Gammarus pulex (Crustacea, Amphipoda)

In Gammarus pulex , male–male competition is generally intense because the operational sex ratio (OSR) is strongly biased towards males; however, studies have shown possible fluctuation in this intrasexual competition, which could be caused by sperm depletion, a phenomenon recently found in gammarids. Sperm depletion may also affect male mating behaviour. We therefore tested the influence of sperm depletion on the OSR in G. pulex . Two sets of experiments were conducted: first, to find out the number of sperm in the testis before and after mating events (sperm depletion), and second, to test the implications of sperm depletion for the mating behaviour of male G. pulex . We found substantial sperm allocation to each reproductive event but also a relatively fast replenishment. However, contrary to one of our hypotheses, sperm depletion had no impact on the male reproductive ‘time-out’ and therefore on the OSR, since depleted males could engage in a precopula within a few hours of a previous copulation. The decision to initiate an amplexus de novo was more dependent on indicators of the females quality such as her time left to moult. Depletion status also did not affect male competitive ability. Indeed, in a competitive context, recently mated G. pulex males were more likely to pair again than those males that had not mated recently, independently of sperm reserves, male size and energy storage. Consequently, some males had better access to reproduction than others, which could be explained by various hypotheses.

Variation between populations and local adaptation in acanthocephalan-induced parasite manipulation.

Many trophically transmitted parasites manipulate their intermediate host phenotype, resulting in higher transmission to the final host. However, it is not known if manipulation is a fixed adaptation of the parasite or a dynamic process upon which selection still acts. In particular, local adaptation has never been tested in manipulating parasites. In this study, using experimental infections between six populations of the acanthocephalan parasite Pomphorhynchus laevis and its amphipod host Gammarus pulex, we investigated whether a manipulative parasite may be locally adapted to its host. We compared adaptation patterns for infectivity and manipulative ability. We first found a negative effect of all parasite infections on host survival. Both parasite and host origins influenced infection success. We found a tendency for higher infectivity in sympatric versus allopatric combinations, but detailed analyses revealed significant differences for two populations only. Conversely, no pattern of local adaptation was found for behavioral manipulation, but manipulation ability varied among parasite origins. This suggests that parasites may adapt their investment in behavioral manipulation according to some of their hosts characteristics. In addition, all naturally infected host populations were less sensitive to parasite manipulation compared to a naive host population, suggesting that hosts may evolve a general resistance to manipulation.

Biological invasion and parasitism: invaders do not suffer from physiological alterations of the acanthocephalan Pomphorhynchus laevis.

Biological invasions expose parasites to new invasive hosts in addition to their local hosts. However, local parasites are often less successful in infecting and exploiting their new hosts. This may have major consequences for the competitive ability of hosts, and finally on the fate of the parasite-host community. In Burgundy (Eastern France), the acanthocephalan parasite, Pomphorhynchus laevis, infects 2 amphipod species living in sympatry: the native Gammarus pulex and the invasive Gammarus roeseli. While P. laevis affects the behaviour and the immunity of G. pulex, G. roeseli seems unaffected by the infection. In this study, we examined in detail the ability of the parasite to affect the immune system and resource storage of both gammarid species. We found that the infection was associated with a general decrease of the prophenoloxidase activity, haemocyte density, resistance to an artificial bacterial infection and level of sugar reserves in G. pulex, but not in G. roeseli. These results demonstrate a differential ability of P. laevis to exploit its local and its invasive gammarid hosts. Potential mechanisms of these differential physiological alterations and their potential consequences on the coexistence of both gammarid species in sympatry are discussed.

Parasite virulence when the infection reduces the host immune response.

Parasite infections often induce a reduction in host immune response either because of a direct manipulation of the immune system by the parasite or because of energy depletion. Although infection-induced immunodepression can favour the establishment of the parasite within the host, a too severe immunodepression may increase the risk of infection with opportunistic pathogens, stopping the period over which the parasite can be transmitted to other hosts. Here, we explore how the risk of contracting opportunistic diseases affects the survival of the amphipod Gammarus pulex infected by the acanthocephalan Pomphorhynchus laevis. Previous work with this system has shown that upon infection, G. pulex has a substantially reduced immune response. Non-infected and P. laevis-infected hosts were maintained either in control or in micro-organism-enriched water, so as to vary the risk of encountering opportunistic pathogens. As predicted, we found that host mortality was exacerbated when infected gammarids were maintained in micro-organism-enriched water compared with clean, control water; whereas for non-infected gammarids, living in micro-organism-enriched water only moderately increased the risk of mortality. These results show that the virulence of parasites that reduce the host immune response is an environmentally sensitive trait that depends on the concomitant risk for the host of contracting opportunistic diseases. This extra source of host mortality probably represents a cost for P. laevis, and we tentatively predict that the optimal level of parasite exploitation should depend on environmental conditions.

Co-variation between the intensity of behavioural manipulation and parasite development time in an acanthocephalan–amphipod system

Pomphorhynchus laevis, a fish acanthocephalan parasite, manipulates the behaviour of its gammarid intermediate host to increase its trophic transmission to the definitive host. However, the intensity of behavioural manipulation is variable between individual gammarids and between parasite populations. To elucidate causes of this variability, we compared the level of phototaxis alteration induced by different parasite sibships from one population, using experimental infections of Gammarus pulex by P. laevis. We used a naive gammarid population, and we carried out our experiments in two steps, during spring and winter. Moreover, we also investigated co‐variation between phototaxis (at different stages of infection, ‘young’ and ‘old cystacanth stage’) and two other fitness‐related traits, infectivity and development time. Three main parameters could explain the parasite intra‐population variation in behavioural manipulation. The genetic variation, suggested by the differences between parasite families, was lower than the variation owing to an (unidentified) environmental factor. Moreover, a correlation was found between development rate and the intensity of behavioural change, the fastest growing parasites being unable to induce rapid phototaxis reversal. This suggests that parasites cannot optimize at the same time these two important parameters of their fitness, and this could explain a part of the variation observed in the wild.

Variation and covariation in infectivity, virulence and immunodepression in the host–parasite association Gammarus pulex–Pomphorhynchus laevis

Parasites often manipulate host immunity for their own benefit, either by exacerbating or suppressing the immune response and this may directly affect the expression of parasite virulence. However, genetic variation in immunodepression, which is a prerequisite to its evolution, and the relationship between immunodepression and virulence, have rarely been studied. Here, we investigated the variation among sibships of the acanthocephalan parasite, Pomphorhynchus laevis, in infecting and in immunodepressing its amphipod host, Gammarus pulex. We also assessed the covariation between infectivity, parasite-induced immune depression and host mortality (parasite virulence). We found that infectivity, the intensity of immunodepression and virulence were variable among parasite sibships. Infectivity and the level of immunodepression were not correlated across parasite sibships. Whereas infectivity was unrelated to host mortality, we found that gammarids that were exposed to the parasite sibships that immunodepressed their hosts the most survived better. This positive covariation between host survival and immunodepression suggests that gammarids exposed to the less immunodepressive parasites could suffer from damage imposed by a higher activity of the phenoloxidase.