Martin Stjernman

Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds

A fragment of the mitochondrial cytochrome b gene of avian malaria (genera Haemoproteus and Plasmodium) was amplified from blood samples of 12 species of passerine birds from the genera Acrocephalus, Phylloscopus and Parus. By sequencing 478 nucleotides of the obtained fragments, we found 17 different mitochondrial haplotypes of Haemoproteus or Plasmodium among the 12 bird species investigated. Only one out of the 17 haplotypes was found in more than one host species, this exception being a haplotype detected in both blue tits (Parus caeruleus) and great tits (Parus major). The phylogenetic tree which was constructed grouped the sequences into two clades, most probably representing Haemoproteus and Plasmodium, respectively. We found two to four different parasite mitochondrial DNA (mtDNA) haplotypes in four bird species. The phylogenetic tree obtained from the mtDNA of the parasites matched the phylogenetic tree of the bird hosts poorly. For example, the two tit species and the willow warbler (Phylloscopus trochilus) carried parasites differing by only 0.6%sequence divergence, suggesting that Haemoproteus shift both between species within the same genus and also between species in different families. Hence, host shifts seem to have occurred repeatedly in this parasite-host system. We discuss this in terms of the possible evolutionary consequences for these bird species.

Transgenerational priming of immunity: maternal exposure to a bacterial antigen enhances offspring humoral immunity

Young vertebrates have limited capacity to synthesize antibodies and are dependent on the protection of maternally transmitted antibodies for humoral disease resistance early in life. However, mothers may enhance fitness by priming their offsprings immune systems to elevate disease resistance. Transgenerational induced defences have been documented in plants and invertebrates, but maternal priming of offspring immunity in vertebrates has been essentially neglected. To test the ability of mothers to stimulate the immune systems of offspring, we manipulated maternal and offspring antigen exposure in a wild population of birds, pied flycatchers (Ficedula hypoleuca). We show that immunization of the mother before egg laying apparently stimulates a transgenerational defence against pathogens by elevating endogenous offspring antibody production. If the disease environments encountered by mothers and offspring are similar, this transgenerational immune priming may allow young to better cope with the local pathogen fauna.

Temperature-dependent costs of parasitism and maintenance of polymorphism under genotype-by-environment interactions.

The maintenance of genetic variation for infection‐related traits is often attributed to coevolution between hosts and parasites, but it can also be maintained by environmental variation if the relative fitness of different genotypes changes with environmental variation. To gain insight into how infection‐related traits are sensitive to environmental variation, we exposed a single host genotype of the freshwater crustacean Daphnia magna to four parasite isolates (which we assume to represent different genotypes) of its naturally co‐occurring parasite Pasteuria ramosa at 15, 20 and 25 °C. We found that the cost to the host of becoming infected varied with temperature, but the magnitude of this cost did not depend on the parasite isolate. Temperature influenced parasite fitness traits; we found parasite genotype‐by‐environment (G × E) interactions for parasite transmission stage production, suggesting the potential for temperature variation to maintain genetic variation in this trait. Finally, we tested for temperature‐dependent relationships between host and parasite fitness traits that form a key component of models of virulence evolution, and we found them to be stable across temperatures.

NATURAL SELECTION ON IMMUNE RESPONSIVENESS IN BLUE TITS PARUS CAERULEUS

Abstract.— What is the form of natural selection on immune responsiveness? For a population at evolutionary equilibrium, there are two different scenarios. First, it is generally assumed that immune defense has both benefits and costs. If variation in immune responsiveness is due to variation in how individuals trade off these costs and benefits, one would expect immune responsiveness to be subject to stabilizing selection. Second, it is well known that an individuals immune responsiveness is often dependent on its overall condition. If immune responsiveness is condition‐dependent, one would expect immune responsiveness to be under positive directional selection. We would therefore expect that the form of natural selection on immune responsiveness depends on the relative magnitude of these two sources of variation: variation in how individuals trade off the costs and benefits of defense, and variation in condition. We measured primary and secondary antibody responsiveness to diphtheria‐tetanus vaccine in blue tits during winter and investigated the relationship between responsiveness and survival to the following breeding season. We use responsiveness to these antigens as measures of an individuals ability or propensity to mount an antibody response in case of an infection. Interestingly, different measures of responsiveness were subject to different selective regimes: primary responsiveness to diphtheria was subject to stabilizing selection, whereas secondary responsiveness to tetanus was subject to positive directional selection. In contrast, there was no significant selection on primary responsiveness to tetanus or secondary responsiveness to diphtheria. The finding of stabilizing selection on a measure of responsiveness is evidence that immune defense can incur fitness costs; a central but little‐tested assumption of theories of the ecology and evolution of immunological defense. The finding of directional selection on a measure of responsiveness is consistent with the idea that immune responsiveness is condition‐dependent, although we cannot rule out the alternative explanation that the population is not at evolutionary equilibrium with respect to this trait.

Immune responsiveness in adult blue tits: heritability and effects of nutritional status during ontogeny.

What is the relative contribution of genetic and various environmental factors to variation in the ability to mount an immune response? We measured antibody responsiveness to diphtheria-tetanus vaccine during the winter in free-ranging blue tits with a known nestling history to investigate (1) if nutritional status during the nestling stage has persistent effects on an individuals immune defence and (2) if immune responsiveness is heritable. There was no correlation between nutritional status during the nestling phase (measured as size-corrected body mass day 14 post-hatch) and antibody responsiveness as an adult. On the other hand, the heritability of responsiveness to diphtheria and tetanus, as estimated by parent-offspring regression, was 0.21±0.51 and 1.21±0.40 SE, respectively. Thus, while there was little evidence that natural variation in antibody responsiveness to these antigens reflected nutritional conditions during early life, responsiveness to at least one of the antigens (tetanus) had a strong genetic component.

Survival costs of reproduction in the blue tit (Parus caeruleus): a role for blood parasites?

One of the central tenets in life–history theory is that there is a trade–off between current and future reproduction (i.e. a cost of reproduction). The mechanism for this cost of reproduction is, however, largely unknown. One hypothesis is that the high workload during reproduction compromises resistance to parasites and that the resulting increase in parasitaemia has negative effects on the prospects of future survival. Although empirical evidence for a negative relationship between reproductive effort and parasite resistance exists, the causal relationships between reproductive effort, parasite resistance and future reproduction are still unclear. We use a path analytical approach to investigate whether a change in parasite resistance (as measured by intensities of infections by the blood parasite Haemoproteus) after manipulation of reproductive effort, translates into altered survival in female blue tits. Our results show a negative relationship between reproductive effort and parasite resistance, although evident only in first–year breeders. Moreover, we found survival costs of reproduction in first–year breeders. These costs were, however, not mediated by the blood parasite studied.

Maximum host survival at intermediate parasite infection intensities.

Background Although parasitism has been acknowledged as an important selective force in the evolution of host life histories, studies of fitness effects of parasites in wild populations have yielded mixed results. One reason for this may be that most studies only test for a linear relationship between infection intensity and host fitness. If resistance to parasites is costly, however, fitness may be reduced both for hosts with low infection intensities (cost of resistance) and high infection intensities (cost of parasitism), such that individuals with intermediate infection intensities have highest fitness. Under this scenario one would expect a non-linear relationship between infection intensity and fitness. Methodology/Principal Findings Using data from blue tits (Cyanistes caeruleus) in southern Sweden, we investigated the relationship between the intensity of infection of its blood parasite (Haemoproteus majoris) and host survival to the following winter. Presence and intensity of parasite infections were determined by microscopy and confirmed using PCR of a 480bp section of the cytochrome-b-gene. While a linear model suggested no relationship between parasite intensity and survival (F = 0.01, p = 0.94), a non-linear model showed a significant negative quadratic effect (quadratic parasite intensity: F = 4.65, p = 0.032; linear parasite intensity F = 4.47, p = 0.035). Visualization using the cubic spline technique showed maximum survival at intermediate parasite intensities. Conclusions/Significance Our results indicate that failing to recognize the potential for a non-linear relationship between parasite infection intensity and host fitness may lead to the potentially erroneous conclusion that the parasite is harmless to its host. Here we show that high parasite intensities indeed reduced survival, but this effect was masked by reduced survival for birds heavily suppressing their parasite intensities. Reduced survival among hosts with low parasite intensities suggests costs of controlling parasite infections; however, the nature of such costs remains to be elucidated.

Genetic variation for maternal effects on parasite susceptibility

The expression of infectious disease is increasingly recognized to be impacted by maternal effects, where the environmental conditions experienced by mothers alter resistance to infection in offspring, independent of heritability. Here, we studied how maternal effects (high or low food availability to mothers) mediated the resistance of the crustacean Daphnia magna to its bacterial parasite Pasteuria ramosa. We sought to disentangle maternal effects from the effects of host genetic background by studying how maternal effects varied across 24 host genotypes sampled from a natural population. Under low‐food conditions, females produced offspring that were relatively resistant, but this maternal effect varied strikingly between host genotypes, i.e. there were genotype by maternal environment interactions. As infection with P. ramosa causes a substantial reduction in host fecundity, this maternal effect had a large effect on host fitness. Maternal effects were also shown to impact parasite fitness, both because they prevented the establishment of the parasites and because even when parasites did establish in the offspring of poorly fed mothers, and they tended to grow more slowly. These effects indicate that food stress in the maternal generation can greatly influence parasite susceptibility and thus perhaps the evolution and coevolution of host–parasite interactions.

MHC-I Affects Infection Intensity but Not Infection Status with a Frequent Avian Malaria Parasite in Blue Tits

Host resistance against parasites depends on three aspects: the ability to prevent, control and clear infections. In vertebrates the immune system consists of innate and adaptive immunity. Innate immunity is particularly important for preventing infection and eradicating established infections at an early stage while adaptive immunity is slow, but powerful, and essential for controlling infection intensities and eventually clearing infections. Major Histocompatibility Complex (MHC) molecules are central in adaptive immunity, and studies on parasite resistance and MHC in wild animals have found effects on both infection intensity (parasite load) and infection status (infected or not). It seems MHC can affect both the ability to control infection intensities and the ability to clear infections. However, these two aspects have rarely been considered simultaneously, and their relative importance in natural populations is therefore unclear. Here we investigate if MHC class I genotype affects infection intensity and infection status with a frequent avian malaria infection Haemoproteus majoris in a natural population of blue tits Cyanistes caeruleus. We found a significant negative association between a single MHC allele and infection intensity but no association with infection status. Blue tits that carry a specific MHC allele seem able to suppress H. majoris infection intensity, while we have no evidence that this allele also has an effect on clearance of the H. majoris infection, a result that is in contrast with some previous studies of MHC and avian malaria. A likely explanation could be that the clearance rate of avian malaria parasites differs between avian malaria lineages and/or between avian hosts.

Long-term effects of nestling condition on blood parasite resistance in blue tits (Cyanistes caeruleus).

Little is know about whether the conditions experienced during ontogeny affect resistance to parasites later in life in wild animals. Here, we used a population of blue tits (Cyanistes caeruleus (L., 1758)) to investigate to what extent conditions experienced during the nestling stage could explain the ability to control blood parasite (Haemoproteus majoris (Laveran, 1902)) infections 1 year later. Although short-term effects may be expected based on the well-known sensitivity of the immune system to current conditions, it is less known whether this translates into a permanent alteration of parasite resistance. By relating nestling condition (measured as body mass or size-corrected body mass) at the beginning and end of the nestling stage to parasite intensity of individual recruiting birds 1 year later, we indeed found significant positive effects of both early and late nestling condition on the long-term ability to control parasites. These results indicate that parasites may be important as a mechanistic explanation for the trade-off between number and quality of offspring. It further points to the potential relevance for maternal effects in host–parasite interactions. (Less)