Paternal hypoxia exposure primes offspring for increased hypoxia resistance.

BACKGROUND: In a time of rapid environmental change, understanding how the challenges experienced by one generation can influence the fitness of future generations is critically needed. Using tolerance assays and transcriptomic and methylome approaches, we use zebrafish as a model to investigate cross-generational acclimation to hypoxia. RESULTS: We show that short-term paternal exposure to hypoxia endows offspring with greater tolerance to acute hypoxia. We detected two hemoglobin genes that are significantly upregulated by more than 6-fold in the offspring of hypoxia exposed males. Moreover, the offspring which maintained equilibrium the longest showed greatest upregulation in hemoglobin expression. We did not detect differential methylation at any of the differentially expressed genes, suggesting that other epigenetic mechanisms are responsible for alterations in gene expression. CONCLUSIONS: Overall, our findings suggest that an epigenetic memory of past hypoxia exposure is maintained and that this environmentally induced information is transferred to subsequent generations, pre-acclimating progeny to cope with hypoxic conditions.

Missing links: testing the completeness of host-parasite checklists.

Host-parasite checklists are essential resources in ecological parasitology, and are regularly used as sources of data in comparative studies of parasite species richness across host species, or of host specificity among parasite species. However, checklists are only useful datasets if they are relatively complete, that is, close to capturing all host-parasite associations occurring in a particular region. Here, we use three approaches to assess the completeness of 25 checklists of metazoan parasites in vertebrate hosts from various geographic regions. First, treating checklists as interaction networks between a set of parasite species and a set of host species, we identify networks with a greater connectance (proportion of realized host-parasite associations) than expected for their size. Second, assuming that the cumulative rise over time in the number of known host-parasite associations in a region tends toward an asymptote as their discovery progresses, we attempt to extrapolate the estimated total number of existing associations. Third, we test for a positive correlation between the number of published reports mentioning an association and the time since its first record, which is expected because observing and reporting host-parasite associations are frequency-dependent processes. Overall, no checklist fared well in all three tests, and only three of 25 passed two of the tests. These results suggest that most checklists, despite being useful syntheses of regional host-parasite associations, cannot be used as reliable sources of data for comparative analyses.

Parental experience of a risky environment leads to improved offspring growth rate.

Parasites (or diseases) are a major selective force for the evolution of life history traits and parasite-host evolution. Mothers can show a variety of responses to parasites during pregnancy, with different consequences for them or their offspring. However, whether information in the maternal environment before pregnancy can cause a change in the phenotype of the offspring is unknown. To avoid the confounding effect of pathogens and to reduce the risk of a direct effect of maternal immune system activation, we injected female laboratory mice with lipopolysaccharides (LPS) before they mated. In order to provide constant information on the potential infectious risk of the environment, females were mated with males that were also exposed to LPS before mating. Offspring from immune-challenged parents were larger and grew at a faster rate than offspring from control parents (injected with PBS). Additionally, offspring from immune-challenged parents that suffered the most from inflammation grew at a faster rate than offspring from low suffering parents. Producing heavier offspring that will reach sexual maturity earlier is likely to have fitness benefits for parents and offspring through improved reproductive success.

Unusual change in activity pattern at cool temperature in a reptile (Sphenodon punctatus).

Animals that can be active both during day and night offer unique opportunities to identify factors that influence activity pattern. By experimental manipulations of temperatures under constant photoperiod, we aimed to determine if emergence, activity and thermoregulatory behaviour of juvenile tuatara (Sphenodon punctatus) varied at different temperatures (20°C, 12°C and 5°C). To help clarify its activity pattern, we compared tuatara with two lizard species endemic of the South Island of New Zealand for which activity pattern is known and clearly defined: the nocturnal common gecko Woodworthia "Otago/Southland" and the diurnal McCann׳s skink Oligosoma maccanni. Tuatara showed similar responses to both species of lizards. Similar to the diurnal skinks, tuatara emerged quickly at 20°C and 12°C while nocturnal geckos took more time to emerge. Like nocturnal geckos, tuatara continued to be active at 5°C, but only during the day. Interestingly, tuatara shifted from diurno-nocturnal activity at 20°C and 12°C to being strictly diurnal at 5°C. We suggest that this temperature-dependent strategy maximises their survival during cold periods.

Differences in resource acquisition, not allocation, mediate the relationship between behaviour and fitness: a systematic review and meta-analysis.

Within populations, individuals often show repeatable variation in behaviour, called 'animal personality'. In the last few decades, numerous empirical studies have attempted to elucidate the mechanisms maintaining this variation, such as life-history trade-offs. Theory predicts that among-individual variation in behavioural traits could be maintained if traits that are positively associated with reproduction are simultaneously associated with decreased survival, such that different levels of behavioural expression lead to the same net fitness outcome. However, variation in resource acquisition may also be important in mediating the relationship between individual behaviour and fitness components (survival and reproduction). For example, if certain phenotypes (e.g. dominance or aggressiveness) are associated with higher resource acquisition, those individuals may have both higher reproduction and higher survival, relative to others in the population. When individuals differ in their ability to acquire resources, trade-offs are only expected to be observed at the within-individual level (i.e. for a given amount of resource, if an individual increases its allocation to reproduction, it comes at the cost of allocation to survival, and vice versa), while among individuals traits that are associated with increased survival may also be associated with increased reproduction. We performed a systematic review and meta-analysis, asking: (i) do among-individual differences in behaviour reflect among-individual differences in resource acquisition and/or allocation, and (ii) is the relationship between behaviour and fitness affected by the type of behaviour and the testing environment? Our meta-analysis consisted of 759 estimates from 193 studies. Our meta-analysis revealed a positive correlation between pairs of estimates using both survival and reproduction as fitness proxies. That is, for a given study, behaviours that were associated with increased reproduction were also associated with increased survival, suggesting that variation in behaviour at the among-individual level largely reflects differences among individuals in resource acquisition. Furthermore, we found the same positive correlation between pairs of estimates using both survival and reproduction as fitness proxies at the phenotypic level. This is significant because we also demonstrated that these phenotypic correlations primarily reflect within-individual correlations. Thus, even when accounting for among-individual differences in resource acquisition, we did not find evidence of trade-offs at the within-individual level. Overall, the relationship between behaviour and fitness proxies was not statistically different from zero at the among-individual, phenotypic, and within-individual levels; this relationship was not affected by behavioural category nor by the testing condition. Our meta-analysis highlights that variation in resource acquisition may be more important in driving the relationship between behaviour and fitness than previously thought, including at the within-individual level. We suggest that this may come about via heterogeneity in resource availability or age-related effects, with higher resource availability and/or age leading to state-dependent shifts in behaviour that simultaneously increase both survival and reproduction. We emphasize that future studies examining the mechanisms maintaining behavioural variation in populations should test the link between behavioural expression and resource acquisition - both within and among individuals. Such work will allow the field of animal personality to develop specific predictions regarding the mediating effect of resource acquisition on the fitness consequences of individual behaviour.

The energetic costs of sub-lethal helminth parasites in mammals: a meta-analysis.

Parasites, by definition, have a negative effect on their host. However, in wild mammal health and conservation research, sub-lethal infections are commonly assumed to have negligible health effects unless parasites are present in overwhelming numbers. Here, we propose a definition for host health in mammals that includes sub-lethal effects of parasites on the host's capacity to adapt to the environment and maintain homeostasis. We synthesized the growing number of studies on helminth parasites in mammals to assess evidence for the relative magnitude of sub-lethal effects of infection across mammal taxa based on this expanded definition. Specifically, we develop and apply a framework for organizing disparate metrics of parasite effects on host health and body condition according to their impact on an animal's energetic condition, defined as the energetic burden of pathogens on host physiological and behavioural functions that relate directly to fitness. Applying this framework within a global meta-analysis of helminth parasites in wild, laboratory and domestic mammal hosts produced 142 peer-reviewed studies documenting 599 infection-condition effects. Analysing these data within a multiple working hypotheses framework allowed us to evaluate the relative weighted contribution of methodological (study design, sampling protocol, parasite quantification methods) and biological (phylogenetic relationships and host/parasite life history) moderators to variation in the magnitude of health effects. We found consistently strong negative effects of infection on host energetic condition across taxonomic groups, with unusually low heterogeneity in effect sizes when compared with other ecological meta-analyses. Observed effect size was significantly lower within cross-sectional studies (i.e. observational studies that investigated a sub-set of a population at a single point in time), the most prevalent methodology. Furthermore, opportunistic sampling led to a weaker negative effect compared to proactive sampling. In the model of host taxonomic group, the effect of infection on energetic condition in carnivores was not significant. However, when sampling method was included, it explained substantial inter-study variance; proactive sampling showing a strongly significant negative effect while opportunistic sampling detected only a weak, non-significant effect. This may partly underlie previous assumptions that sub-lethal parasites do not have significant effects on host health. We recommend future studies adopt energetic condition as the framework for assessing parasite effects on wildlife health and provide guidelines for the selection of research protocols, health proxies, and relating infection to fitness.

Thermal dependence of locomotor performance in two cool-temperate lizards.

Temperate-zone ectotherms experience varying or very low ambient temperatures and may have difficulty in attaining preferred body temperatures. Thus, adaptations to reduce the thermal dependence of physiological processes may be present. We measured the optimal temperature range for sprint speed and compared it with the selected body temperatures (T (sel)) of two sympatric, cool-temperate lizards: the diurnal skink Oligosoma maccanni and the primarily nocturnal gecko Woodworthia (previously Hoplodactylus) "Otago/Southland". We also investigated whether time-of-day influenced sprint speed. Contrary to results for other reptiles, we found that time-of-day did not influence speed in either species. For each species, the optimal temperature range for sprinting and T (sel) overlapped, supporting the 'thermal coadaptation' hypothesis. However, the optimal range of temperatures for speed is not always attainable during activity by either species, which have limited opportunities to attain T (sel) in the field. The thermal sensitivity of sprint speed in these two species does not appear to have evolved to fully match their current thermal environment. More data on cold-adapted species are needed to fully understand physiological adaptation in ectotherms.

Effect of maternal diet on offspring coping styles in rodents: a systematic review and meta-analysis.

Maternal nutrition can have long-term effects on offspring morphology, physiology and behaviours. However, it is unclear whether mothers 'program' offspring behavioural coping strategy (proactive/reactive) according to the predicted nutritional quality of their future environment. We conducted a systematic review on this topic and meta-analytically synthesized relevant experimental data on mice and rats (46 studies). We included data from experiments where dams were subjected to caloric restriction, protein restriction or overfeeding around gestation and subsequently measured offspring activity, exploration, or anxiety. Overall, little evidence existed for effects of maternal nutrition on the three investigated behavioural traits. The high heterogeneity observed in the data set suggests that maternal programming may sometimes occur. However, because offspring had access to a balanced diet before testing, behaviours may have been reprogrammed. Our results may indicate that reprogrammed behaviours could ameliorate negative effects associated with sub-optimal nutrition in early life. Further, our systematic review revealed clear knowledge gaps and fruitful future research avenues.

Correlational selection on pro- and anti-inflammatory effectors.

Parasites impose a permanent threat for hosts. As a consequence, immune defenses are important for host fitness. However, the immune response can also produce self-damage and impair host fitness if not properly regulated. Effectors that up- and downregulate the immune response should, therefore, evolve in concert, and be under the action of correlational selection. To address this issue, we assessed the shape of the selection operating on pro- and anti-inflammatory effectors following an inflammatory challenge in laboratory mice.We found that selection acts on the combination of these two traits as individuals that produced large amount of pro-inflammatory cytokines could achieve relatively high fitness (survival) only if also producing a large amount of anti-inflammatory effectors. To our knowledge, this is the first study providing evidence for correlational selection on immunity.