Grandparental effects in marine sticklebacks: transgenerational plasticity across multiple generations.

Nongenetic inheritance mechanisms such as transgenerational plasticity (TGP) can buffer populations against rapid environmental change such as ocean warming. Yet, little is known about how long these effects persist and whether they are cumulative over generations. Here, we tested for adaptive TGP in response to simulated ocean warming across parental and grandparental generations of marine sticklebacks. Grandparents were acclimated for two months during reproductive conditioning, whereas parents experienced developmental acclimation, allowing us to compare the fitness consequences of short-term vs. prolonged exposure to elevated temperature across multiple generations. We found that reproductive output of F1 adults was primarily determined by maternal developmental temperature, but carry-over effects from grandparental acclimation environments resulted in cumulative negative effects of elevated temperature on hatching success. In very early stages of growth, F2 offspring reached larger sizes in their respective paternal and grandparental environment down the paternal line, suggesting that other factors than just the paternal genome may be transferred between generations. In later growth stages, maternal and maternal granddam environments strongly influenced offspring body size, but in opposing directions, indicating that the mechanism(s) underlying the transfer of environmental information may have differed between acute and developmental acclimation experienced by the two generations. Taken together, our results suggest that the fitness consequences of parental and grandparental TGP are highly context dependent, but will play an important role in mediating some of the impacts of rapid climate change in this system.

Male mate choice relies on major histocompatibility complex class I in a sex-role-reversed pipefish.

Mate choice for compatible genes is often based on genes of the major histocompatibility complex (MHC). Although MHC-based mate choice is commonly observed in female choice, male mate choice remains elusive. In particular, if males have intense paternal care and are thus the choosing sex, male choice for females with dissimilar MHC can be expected. Here, we investigated whether male mate choice relies on MHC class I genes in the sex-role reversed pipefish Syngnathus typhle. In a mate choice experiment, we determined the relative importance of visual and olfactory cues by manipulating visibility and olfaction. We found that pipefish males chose females that maximize sequence-based amino acid distance between MHC class I genotypes in the offspring when olfactory cues were present. Under visual cues, large females were chosen, but in the absence of visual cues, the choice pattern was reversed. The use of sex-role reversed species thus revealed that sexual selection can lead to the evolution of male mate choice for MHC class I genes.

Nonlinear effects of temperature on body form and developmental canalization in the threespine stickleback.

Theoretical models predict that nonlinear environmental effects on the phenotype also affect developmental canalization, which in turn can influence the tempo and course of organismal evolution. Here, we used an oceanic population of threespine stickleback (Gasterosteus aculeatus) to investigate temperature-induced phenotypic plasticity of body size and shape using a paternal half-sibling, split-clutch experimental design and rearing offspring under three different temperature regimes (13, 17 and 21 °C). Body size and shape of 466 stickleback individuals were assessed by a set of 53 landmarks and analysed using geometric morphometric methods. At approximately 100 days, individuals differed significantly in both size and shape across the temperature groups. However, the temperature-induced differences between 13 and 17 °C (mainly comprising relative head and eye size) deviated considerably from those between 17 and 21 °C (involving the relative size of the ectocoracoid, the operculum and the ventral process of the pelvic girdle). Body size was largest at 17 °C. For both size and shape, phenotypic variance was significantly smaller at 17 °C than at 13 and 21 °C, indicating that development is most stable at the intermediate temperature matching the conditions encountered in the wild. Higher additive genetic variance at 13 and 21 °C indicates that the plastic response to temperature had a heritable basis. Understanding nonlinear effects of temperature on development and the underlying genetics are important for modelling evolution and for predicting outcomes of global warming, which can lead not only to shifts in average morphology but also to destabilization of development.

Experimental coevolution leads to a decrease in parasite-induced host mortality.

Host-parasite coevolution can lead to a variety of outcomes, but whereas experimental studies on clonal populations have taken prominence over the last years, experimental studies on obligately out-crossing organisms are virtually absent so far. Therefore, we set up a coevolution experiment using four genetically distinct lines of Tribolium castaneum and its natural obligately killing microsporidian parasite, Nosema whitei. After 13 generations of experimental coevolution, we employed a time-shift experiment infecting hosts from the current generation with parasites from nine different time points in coevolutionary history. Although initially parasite-induced mortality showed synchronized fluctuations across lines, a general decrease over time was observed, potentially reflecting evolution towards optimal levels of virulence or a failure to adapt to coevolving sexual hosts.

Host genetic architecture in single and multiple infections.

Hosts are often target to multiple simultaneous infections by genetically diverse parasite strains. The interaction among these strains and the interaction of each strain with the host was shown to have profound effects on the evolution of parasite traits. Host factors like genetic architecture of resistance have so far been largely neglected. To see whether genetic architecture differs between different kinds of infections we used joint scaling analysis to compare the genetic components of resistance in the red flour beetle Tribolium castaneum exposed to single and multiple strains of the microsporidian Nosema whitei. Our results indicate that additive, dominance and epistatic components were more important in single infections whereas maternal components play a decisive role in multiple infections. In detail, parameter estimates of additive, dominance and epistatic components correlated positively between single and multiple infections, whereas maternal components correlated negatively. These findings may suggest that specificity of host-parasite interactions are mediated by genetic and especially epistatic components whereas maternal effects constitute a more general form of resistance.

Genetic variation in MHC class II expression and interactions with MHC sequence polymorphism in three-spined sticklebacks.

Genes of the major histocompatibility complex (MHC) have been studied for several decades because of their pronounced allelic polymorphism. Structural allelic polymorphism is, however, not the only source of variability subjected to natural selection. Genetic variation may also exist in gene expression patterns. Here, we show that in a natural population of three-spined sticklebacks (Gasterosteus aculeatus) the expression of MHC class IIB genes was positively correlated with parasite load, which indicates increased immune activation of the MHC when infections are frequent. To experimentally study MHC expression, we used laboratory-bred sticklebacks that were exposed to three naturally occurring species of parasite. We found strong differences in MHC class IIB expression patterns among fish families, which were consistent over two generations, thus demonstrating a genetic component. The average number of MHC class IIB sequence variants within families was negatively correlated to the MHC expression level suggesting compensatory up-regulation in fish with a low (i.e. suboptimal) MHC sequence variability. The observed differences among families and the negative correlation with individual sequence diversity imply that MHC expression is evolutionary relevant for the onset and control of the immune response in natural populations.

Multiple parasites are driving major histocompatibility complex polymorphism in the wild.

Parasite mediated selection may result in arms races between host defence and parasite virulence. In particular, simultaneous infections from multiple parasite species should cause diversification (i.e. balancing selection) in resistance genes both at the population and the individual level. Here, we tested these ideas in highly polymorphic major histocompatibility complex (MHC) genes from three-spined sticklebacks (Gasterosteus aculeatus L.). In eight natural populations, parasite diversity (15 different species), and MHC class IIB diversity varied strongly between habitat types (lakes vs. rivers vs. estuaries) with lowest values in rivers. Partial correlation analysis revealed an influence of parasite diversity on MHC class IIB variation whereas general genetic diversity assessed at seven microsatellite loci was not significantly correlated with parasite diversity. Within individual fish, intermediate, rather than maximal allele numbers were associated with minimal parasite load, supporting theoretical models of self-reactive T-cell elimination. The optimal individual diversity matched those values female fish try to achieve in their offspring by mate choice. We thus present correlative evidence supporting the 'allele counting' strategy for optimizing the immunocompetence in stickleback offspring.

Rapid genetic divergence in postglacial populations of threespine stickleback (Gasterosteus aculeatus): the role of habitat type, drainage and geographical proximity.

The goal of this study was to evaluate the role of common ancestry, and of geographical or reproductive isolation, in genetic divergence in populations of threespine sticklebacks (Gasterosteus aculeatus). Using seven DNA microsatellite loci we compared the effects of habitat type, drainage system and geographical proximity on genetic distance among 16 populations situated in an area in Schleswig-Holstein (Germany) that became deglaciated approximately 12 000 years ago. Stickleback population structure correlated only weakly with drainage system, whereas the primary divergence was among habitat types. Phylogenetic analysis revealed that lake (n = 7) and river (n = 5) populations formed two distinct clades (Cavalli-Sforza's and Edwards' chord distance, 82-100% bootstrap support) at approximately equal genetic distances to a third clade, comprising putative estuarine (n = 4) ancestors. Allele frequencies in lake and river populations represented different subsets of the genetically more diverse estuarine populations. In nested amovas approximately twice the genetic variance was distributed among lake vs. river vs. estuarine populations as compared with the combined effects of drainage system and geographical distance. Limited gene flow between habitat types must have been established after postglacial colonization, suggesting ecological hybrid inferiority or behavioural mating barriers between ecotypes. Within estuarine and lake populations, population differentiation followed an isolation-by-distance model. Given the high observed heterozygosities within the 16 study populations (HO = 0.65-0.87), the mean divergence between lake and river population pairs (FST = 0.18 +/- 0.007) would be reached after 300-6000 generations in a stepwise mutation model, depending on the size of N(e). This demonstrates both the utility of hypervariable microsatellites for detecting recent population divergences and the danger of operating at temporal or spatial scales which are beyond their resolution.