Episodes of opposing survival and reproductive selection cause strong fluctuating selection on seasonal migration versus residence

Quantifying temporal variation in sex-specific selection on key ecologically relevant traits, and quantifying how such variation arises through synergistic or opposing components of survival and reproductive selection, is central to understanding eco-evolutionary dynamics, but rarely achieved. Seasonal migration versus residence is one key trait that directly shapes spatio-seasonal population dynamics in spatially and temporally varying environments, but temporal dynamics of sex-specific selection have not been fully quantified. We fitted multi-event capture–recapture models to year-round ring resightings and breeding success data from partially migratory European shags ( Phalacrocorax aristotelis ) to quantify temporal variation in annual sex-specific selection on seasonal migration versus residence arising through adult survival, reproduction and the combination of both (i.e. annual fitness). We demonstrate episodes of strong and strongly fluctuating selection through annual fitness that were broadly synchronized across females and males. These overall fluctuations arose because strong reproductive selection against migration in several years contrasted with strong survival selection against residence in years with extreme climatic events. These results indicate how substantial phenotypic and genetic variation in migration versus residence could be maintained, and highlight that biologically important fluctuations in selection may not be detected unless both survival selection and reproductive selection are appropriately quantified and combined.

Evolution of epigenetic transmission when selection acts on fecundity versus viability

Existing theory on the evolution of parental effects and the inheritance of non-genetic factors has mostly focused on the role of environmental change. By contrast, how differences in population demography and life history affect parental effects is poorly understood. To fill this gap, we develop an analytical model to explore how parental effects evolve when selection acts on fecundity versus viability in spatio-temporally fluctuating environments. We find that regimes of viability selection, but not fecundity selection, are most likely to favour parental effects. In the case of viability selection, locally adapted phenotypes have a higher survival than maladapted phenotypes and hence become enriched in the local environment. Hence, simply by being alive, a parental phenotype becomes correlated to its environment (and hence informative to offspring) during its lifetime, favouring the evolution of parental effects. By contrast, in regimes of fecundity selection, correlations between phenotype and environment develop more slowly: this is because locally adapted and maladapted parents survive at equal rates (no survival selection), so that parental phenotypes, by themselves, are uninformative about the local environment. However, because locally adapted parents are more fecund, they contribute more offspring to the local patch than maladapted parents. In case these offspring are also likely to inherit the adapted parents’ phenotypes (requiring pre-existing inheritance), locally adapted offspring become enriched in the local environment, resulting in a correlation between phenotype and environment, but only in the offspring’s generation. Because of this slower build-up of a correlation between phenotype and environment essential to parental effects, fecundity selection is more sensitive to any distortions owing to environmental change than viability selection. Hence, we conclude that viability selection is most conducive to the evolution of parental effects. This article is part of the theme issue ‘How does epigenetics influence the course of evolution?’

High heritability of telomere length, but low evolvability, and no significant heritability of telomere shortening in wild jackdaws

Telomere length (TL) and shortening rate predict survival in many organisms. Evolutionary dynamics of TL in response to survival selection depend on the presence of genetic variation that selection can act upon. However, the amount of standing genetic variation is poorly known for both TL and TL shortening rate, and has not been studied for both traits in combination in a wild vertebrate. We used experimental (cross-fostering) and statistical (animal models) means to disentangle and estimate genetic and environmental contributions to TL variation in pedigreed free-living jackdaws (Corvus monedula). TL was measured twice early in life (age- and interval-standardized), when shortening is highest, using the high-precision TRF technique, adapted to exclude interstitial telomeric sequences. TL shortened significantly during the nestling phase (10.4 bp/day), was highly repeatable within individuals (R=0.97) and genetically correlated between the two ages (rG>0.99). Additive genetic effects explained the major part of TL variation between individuals, with heritability on average estimated at h2=0.74. Parent- offspring regressions yielded similar estimates for the sexes when accounting for changes in paternal TL over life. Cohort effects explained a small but significant part of TL variation. Heritable variation for telomere shortening was negligible. Despite the high heritability of TL, its evolvability, which scales the additive genetic variance by mean TL, was close to zero. Hence evolutionary change of TL is likely to be slow despite significant selection.

Origin of DNA Repair in the RNA World

The early history of life on Earth likely included a stage in which life existed as self-replicating protocells with single-stranded RNA (ssRNA) genomes. In this RNA world, genome damage from a variety of sources (spontaneous hydrolysis, UV, etc.) would have been a problem for survival. Selection pressure for dealing with genome damage would have led to adaptive strategies for mitigating the damage. In today’s world, RNA viruses with ssRNA genomes are common, and these viruses similarly need to cope with genome damage. Thus ssRNA viruses can serve as models for understanding the early evolution of genome repair. As the ssRNA protocells in the early RNA world evolved, the RNA genome likely gave rise, through a series of evolutionary stages, to the double-stranded DNA (dsDNA) genome. In ssRNA to dsDNA evolution, genome repair processes also likely evolved to accommodate this transition. Some of the basic features of ssRNA genome repair appear to have been retained in descendants with dsDNA genomes. In particular, a type of strand-switching recombination occurs when ssRNA replication is blocked by a damage in the template strand. Elements of this process appear to have a central role in recombinational repair processes during meiosis and mitosis of descendant dsDNA organisms.

Sex-dependent expression of behavioural genetic architectures and the evolution of sexual dimorphism

Empirical studies imply that sex-specific genetic architectures can resolve evolutionary conflicts between males and females, and thereby facilitate the evolution of sexual dimorphism. Sex-specificity of behavioural genetic architectures has, however, rarely been considered. Moreover, as the expression of genetic (co)variances is often environment-dependent, general inferences on sex-specific genetic architectures require estimates of quantitative genetics parameters under multiple conditions. We measured exploration and aggression in pedigreed populations of southern field crickets ( Gryllus bimaculatus ) raised on either naturally balanced (free-choice) or imbalanced (protein-deprived) diets. For each dietary condition, we measured for each behavioural trait (i) level of sexual dimorphism, (ii) level of sex-specificity of survival selection gradients, (iii) level of sex-specificity of additive genetic variance, and (iv) strength of the cross-sex genetic correlation. We report here evidence for sexual dimorphism in behaviour as well as sex-specificity in the expression of genetic (co)variances as predicted by theory. The additive genetic variances of exploration and aggression were significantly greater in males compared with females. Cross-sex genetic correlations were highly positive for exploration but deviating (significantly) from one for aggression; findings were consistent across dietary treatments. This suggests that genetic architectures characterize the sexually dimorphic focal behaviours across various key environmental conditions in the wild. Our finding also highlights that sexual conflict can be resolved by evolving sexually independent genetic architectures.

Pale and dark morphs of tawny owls show different patterns of telomere dynamics in relation to disease status

Parasites are expected to exert long-term costs on host fecundity and longevity. Understanding the consequences of heritable polymorphic variation in disease defence in wild populations is essential in order to predict evolutionary responses to changes in disease risk. Telomeres have been found to shorten faster in malaria-diseased individuals compared with healthy ones with negative effects on longevity and thereby fitness. Here, we study the impact of haemosporidian blood parasites on telomere dynamics in tawny owls, which display a highly heritable plumage colour polymorphism. Previously, it has been shown that blood parasites have morph-specific impact on body mass maintenance. Here, we show that telomeres shortened faster in individuals with shorter breeding lifespan. Telomere length was negatively associated with the degree of pheomelanic brown coloration and shorter in infected than uninfected individuals. The rate of telomere shortening between breeding seasons was faster in darker pheomelanic individuals and suppression of parasite intensity between seasons was associated with faster telomere shortening in the paler individuals but not in darker ones. We propose that morph-specific physiological profiles cause differential telomere shortening and that this is likely to be a mechanism involved in previously documented environment-driven survival selection against the pheomelanic morph in this population.