Description: Trans-generational plasticity is the adjustment of phenotypes to changing habitat conditions that persist longer than the individual lifetime. Fitness benefits (adaptive TGP) are expected upon matching parent-offspring environments. In a global change scenario, several performance-related environmental factors are changing simultaneously. This lowers the predictability of offspring environmental conditions, potentially hampering the benefits of trans-generational plasticity. For the first time, we here explore how the combination of an abiotic and a biotic environmental factor in the parental generation plays out as trans-generational effect in the offspring. We fully reciprocally exposed the parental generation of the pipefish Syngnathus typhle to an immune challenge and elevated temperatures simulating a naturally occurring heatwave. Upon mating and male pregnancy, offspring were kept in ambient or elevated temperature regimes combined with a heat-killed bacterial epitope treatment. Differential gene expression (immune genes and DNA- and histone-modification genes) suggests that the combined change of an abiotic and a biotic factor in the parental generation had interactive effects on offspring performance, the temperature effect dominated over the immune challenge impact. The benefits of certain parental environmental conditions on offspring performance did not sum up when abiotic and biotic factors were changed simultaneously supporting that available resources are limited that can be allocated to phenotypic trans-generational effects. Temperature is the master regulator of trans-generational phenotypic plasticity, which potentially implies a conflict in the allocation of resources towards several environmental factors. This asks for a reassessment of trans-generational plasticity as a short-term option to buffer environmental variation in the light of climate change.

Description: Given the ubiquity of the parasites and their important fitness consequences on mate and offspring condition, selection for the ability to distinguish healthy from parasitized potential mates is a key process to enhance Darwinian fitness. In this study, we experimentally evaluated how the immunological experience of two potential partners influences mate choice, using the sex-role-reversed pipefish Syngnathus typhle. We exposed S. typhle to immune challenges with heat-killed Vibrio bacteria and investigated whether the activation of the immune system determined mate preferences. Our results demonstrate that the immune status of the potential partners influenced female mate preference, such that females that were exposed to an immune challenge became choosy and favored unchallenged males. Males, however, did not show any preferences for female immune status. In this context, we discuss mate choice decisions and behavioral plasticity as a complex result of immune challenge, severity of infection, as well as trans-generational effects.

Description: Animals can profit from increasing temperatures by prolonged breeding seasons and faster growth rates. However, these fitness benefits are traded off against higher parasite load and increased virulence of temperature-sensitive pathogens. In thermally stratified habitats, behavioral plasticity can allow hosts to choose the optimal temperature to enhance individual fitness and to escape parasite pressure. To test this idea, we performed a temperature choice experiment with the host-parasite system of the sex-role reversed broad-nosed pipefish (Syngnathus typhle) and its bacterial pathogen Vibrio spp. In this species, pregnant males are expected to face a trade-off between shortening their brooding period in warm water and decreasing the effect of the infection in cold water. We found that exposure to Vibrio changed the temperature preference for both pregnant and nonpregnant males, as well as females compared to nonchallenged fish that tended to prefer warm water. This study shows that behavioral plasticity is one option for avoidance of higher bacterial prevalence, as expected due to rising ocean temperatures.

Description: Given the ubiquity of the parasites and their important fitness consequences on mate and offspring condition, selection for the ability to distinguish healthy from parasitized potential mates is a key process to enhance Darwinian fitness. In this study, we experimentally evaluated how the immunological experience of two potential partners influences mate choice, using the sex-role-reversed pipefish Syngnathus typhle. We exposed S. typhle to immune challenges with heat-killed Vibrio bacteria and investigated whether the activation of the immune system determined mate preferences. Our results demonstrate that the immune status of the potential partners influenced female mate preference, such that females that were exposed to an immune challenge became choosy and favored unchallenged males. Males, however, did not show any preferences for female immune status. In this context, we discuss mate choice decisions and behavioral plasticity as a complex result of immune challenge, severity of infection, as well as trans-generational effects.

Description: Extreme climate events such as heat waves are expected to increase in frequency under global change. As one indirect effect, they can alter magnitude and direction of species interactions, for example those between hosts and parasites. We simulated a summer heat wave to investigate how a changing environment affects the interaction between the broad-nosed pipefish (Syngnathus typhle) as a host and its digenean trematode parasite (Cryptocotyle lingua). In a fully reciprocal laboratory infection experiment, pipefish from three different coastal locations were exposed to sympatric and allopatric trematode cercariae. In order to examine whether an extreme climatic event disrupts patterns of locally adapted host-parasite combinations we measured the parasite's transmission success as well as the host's adaptive and innate immune defence under control and heat wave conditions. Independent of temperature, sympatric cercariae were always more successful than allopatric ones, indicating that parasites are locally adapted to their hosts. Hosts suffered from heat stress as suggested by fewer cells of the adaptive immune system (lymphocytes) compared to the same groups that were kept at 18°C. However, the proportion of the innate immune cells (monocytes) was higher in the 18°C water. Contrary to our expectations, no interaction between host immune defence, parasite infectivity and temperature stress were found, nor did the pattern of local adaptation change due to increased water temperature. Thus, in this host-parasite interaction, the sympatric parasite keeps ahead of the coevolutionary dynamics across sites, even under increasing temperatures as expected under marine global warming.

Description: Microparasites have a higher evolutionary potential than their hosts due to an increased mutation rate and a shorter generation time that usually results in parasites being locally adapted to their sympatric hosts. This pattern may not apply to generalist pathogens as adaptation to sympatric host genotypes is disadvantageous due to a narrowing of the host range, in particular under strong gene flow among host populations. Under this scenario, we predict that the immune defense of hosts reveals adaptation to locally common pathogen phylotypes. This was tested in four host populations of the pipefish Syngnathus typhle and associated bacteria of the genus Vibrio. We investigated the population divergence among host and bacteria populations and verified that gene flow is higher among host populations than among parasite populations. Next, we experimentally assessed the strength of innate immune defense of pipefish hosts using in vitro assays that measured antimicrobial activity of blood plasma against sympatric and allopatric Vibrio phylotypes. Pipefish plasma displays stronger antimicrobial activity against sympatric Vibrio phylotypes compared to allopatric ones. This suggests that host defense is genetically adapted against local bacteria with a broad and unspecialized host spectrum, a situation that is typical for marine systems with weak host population structure.

Description: Trans-generational plasticity is the adjustment of phenotypes to changing habitat conditions that persist longer than the individual lifetime. Fitness benefits (adaptive TGP) are expected upon matching parent-offspring environments. In a global change scenario, several performance-related environmental factors are changing simultaneously. This lowers the predictability of offspring environmental conditions, potentially hampering the benefits of trans-generational plasticity. For the first time, we here explore how the combination of an abiotic and a biotic environmental factor in the parental generation plays out as trans-generational effect in the offspring. We fully reciprocally exposed the parental generation of the pipefish Syngnathus typhle to an immune challenge and elevated temperatures simulating a naturally occurring heatwave. Upon mating and male pregnancy, offspring were kept in ambient or elevated temperature regimes combined with a heat-killed bacterial epitope treatment. Differential gene expression (immune genes and DNA- and histone-modification genes) suggests that the combined change of an abiotic and a biotic factor in the parental generation had interactive effects on offspring performance, the temperature effect dominated over the immune challenge impact. The benefits of certain parental environmental conditions on offspring performance did not sum up when abiotic and biotic factors were changed simultaneously supporting that available resources that can be allocated to phenotypic trans-generational effects are limited. Temperature is the master regulator of trans-generational phenotypic plasticity, which potentially implies a conflict in the allocation of resources towards several environmental factors. This asks for a reassessment of trans-generational plasticity as a short-term option to buffer environmental variation in the light of climate change.

Description: Species interactions are among the most important forces structuring ecological communities (Chesson 2000, Wilson et al. 2003). Current and forecasted temperature shifts will affect interacting species and with that entire ecosystems thus the study of evolutionary potential to cope with a changing world became a key challenge (Paull et al. 2012, Munday et al. 2013). Special attention must be paid to host-parasite interactions, because temperature changes have the potential to increase the global distribution and prevalence of infectious diseases to the detriment of human health, biodiversity, and population structures (Harvell et al. 2002, Lafferty 2009, Rohr et al. 2011, Burge et al. 2014). Yet, disease dynamics of marine pathogens under the influence of a changing climate are not well understood, mainly due to the challenge to study wild, often mobile organisms in a large system where direct observation is not feasible (Burge et al. 2014). In my thesis, I focused on host-parasite interactions between the ubiquitous pipefish Syngnathus typhle with two of its common parasites Cryptocotyle lingua and Vibrio in the Baltic Sea. This region is predicted to be affected stronger than the global average by warming and climate extremes, such as heat waves (Stigebrandt & Gustafsson 2003, Belkin 2009, Baker-Austin et al. 2013). I wanted to find out how forecasted temperature shifts might affect a host-parasite interaction. Moreover, I wanted to examine the phenotypic plastic potential of S. typhle to cope with infections and a warming ocean. I therefore combined during my PhD extensive field sampling, molecular biology, and immunological methods with controlled infection and behaviour experiments. As a first step, I described a status quo of interacting host-parasite pairs that were collected at several geographically distinct locations. These interactions, shaped by co-evolution and natural selection, are reflected in local adaptation mosaics between host and parasite (Gomulkiewicz et al. 2000). I could detect local parasite adaptation of C. lingua to S. typhle, but local host adaptation of S. typhle to Vibrio. Thus one host shares differing patterns of local adaptation with its parasites, which remain constant over geographic distribution. This finding illustrates the high complexity of host-parasite interactions. The status quo of local adaptation patterns served as baseline for my next experiment: Can a heat wave disrupt a co-evolved host-parasite interaction because one of the interacting partners might benefit from higher temperatures? For this, I imposed an experimental heat wave on the host-parasite system of S. typhle – C. lingua. The pattern of local adaptation was not disrupted. Alarmingly, S. typhle’s adaptive immune defence was delayed during the experimental heat wave, showing that an extreme weather event could predispose a natural population to disease outbreak. Surprisingly, infection success of the parasite was not influenced by the heat wave indicating that local adaptation between host and parasite genotypes might be more important than first order temperature effects on the parasite. As many other marine ectothermic organisms, I could show that pipefish are affected by temperature shifts due to an impaired immune response (Landis et al. 2012b, Burge et al. 2014). Additionally, the predicted emergence and the increased risk of disease outbreak of the bacterial pathogen Vibrio in the Baltic Sea (Baker-Austin et al. 2013) draws a dark future for local pipefish. Yet, pipefish are motile organisms and thus might be able to cope with a warming environment and emerging diseases by behavioural acclimatization (“behavioural chills”), i.e. by choosing a more suitable, cooler environment. To test this, I measured the behavioural plasticity of healthy and immune challenged fish. Infected pipefish showed a significant preference for cooler water. The choice of a cooler environment upon immune challenge therefore has a twofold benefit: immune defence of pipefish is not compromised thus an existing infection can be cleared, and the parasite faces a non-optimal temperature niche (Landis et al. 2012a, Baker-Austin et al. 2013). To further investigate this species interaction, I examined, if pipefish are not only able to fight their infections with behavioural chills, but if they also avoid mates that are immune challenged with the same bacterium. In a mate choice experiment I tested if pipefish can recognize immune status of their mates and if immune status influences their mate choice. Healthy females did not discriminate between infected and naïve males, possibly to enhance short-time mating success. Upon immune challenge, females became choosy and showed a preference for unchallenged males, which could increase offspring’s fitness. Independent of the immunological treatment, males remained indifferent towards the immune challenge of females. These results provide experimental evidence to a growing body of work (Chevin et al. 2010, Bonduriansky et al. 2012, Munday et al. 2013, Nemeth et al. 2013, Crozier & Hutchings 2014), showing that phenotypic plasticity may help buffer populations against the immediate impacts of environmental change. These plastic adaptations are crucial as they can provide the time needed for genetic adaptation to a changing world.