Molecular basis of parental contributions to the behavioural tolerance of elevated pCO 2 in a coral reef fish

Knowledge of adaptive potential is crucial to predicting the impacts of ocean acidification (OA) on marine organisms. In the spiny damselfish, Acanthochromis polyacanthus , individual variation in behavioural tolerance to elevated pCO 2 has been observed and is associated with offspring gene expression patterns in the brain. However, the maternal and paternal contributions of this variation are unknown. To investigate parental influence of behavioural pCO 2 tolerance, we crossed pCO 2 -tolerant fathers with pCO 2 -sensitive mothers and vice versa, reared their offspring at control and elevated pCO 2 levels, and compared the juveniles' brain transcriptional programme. We identified a large influence of parental phenotype on expression patterns of offspring, irrespective of environmental conditions. Circadian rhythm genes, associated with a tolerant parental phenotype, were uniquely expressed in tolerant mother offspring, while tolerant fathers had a greater role in expression of genes associated with histone binding. Expression changes in genes associated with neural plasticity were identified in both offspring types: the maternal line had a greater effect on genes related to neuron growth while paternal influence impacted the expression of synaptic development genes. Our results confirm cellular mechanisms involved in responses to varying lengths of OA exposure, while highlighting the parental phenotype's influence on offspring molecular phenotype.

Epigenetically Inherited Mutation Rates Predicted to Maximize Adaptation Rates

The mutation rate is an important determinant of evolutionary dynamics. Because the mutation rate determines the rate of appearance of beneficial and deleterious mutations, it is subject to second-order selection. The mutation rate varies between and within species and populations, increases under stress, and is genetically controlled by mutator alleles. The mutation rate may also vary among genetically identical individuals: empirical evidence from bacteria suggests that the mutation rate may be affected by translation errors and expression noise in various proteins (1). Importantly, this non-genetic variation may be heritable via transgenerational epigenetic inheritance. Here we investigate how the inheritance mode of the mutation rate affects the rate of adaptive evolution on rugged fitness landscapes. We model an asexual population with two mutation rate phenotypes, non-mutator and mutator. An offspring may switch from its parental phenotype to the other phenotype. The rate of switching between the mutation rate phenotypes is allowed to span a range of values. Thus, the mutation rate can be interpreted as a genetically inherited trait when the switching rate is low, as an epigenetically inherited trait when the switching rate is intermediate, or as a randomly determined trait when the switching rate is high. We find that epigenetically inherited mutation rates result in the highest rates of adaptation on rugged fitness landscapes for most realistic parameter sets. This is because an intermediate switching rate can maintain the association between a mutator phenotype and pre-existing mutations, which facilitates the crossing of fitness valleys. Our results provide a rationale for the evolution of epigenetic inheritance of the mutation rate, suggesting that it could have been selected because it facilitates adaptive evolution.

No evidence for increased fitness of offspring from multigenerational effects of parental size or natal carcass size in the burying beetle Nicrophorus marginatus

Multigenerational effects (often called maternal effects) are components of the offspring phenotype that result from the parental phenotype and the parental environment as opposed to heritable genetic effects. Multigenerational effects are widespread in nature and are often studied because of their potentially important effects on offspring traits. Although multigenerational effects are commonly observed, few studies have addressed whether they affect offspring fitness. In this study we assess the effect of potential multigenerational effects of parental body size and natal carcass size on lifetime fitness in the burying beetle, Nicrophorus marginatus (Coleoptera; Silphidae). Lifespan, total number of offspring, and number of offspring in the first reproductive bout were not significantly related to parental body size or natal carcass size. However, current carcass size used for reproduction was a significant predictor for lifetime number of offspring and number of offspring in the first brood. We find no evidence that multigenerational effects from larger parents or larger natal carcasses contribute to increased fitness of offspring.

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?’

Intergenerational Effects of Early Life Starvation on Life-History, Consumption, and Transcriptome of a Holometabolous Insect

ABSTRACTIntergenerational effects, also known as parental effects in which the offspring phenotype is influenced by the parental phenotype, can occur in response to parental early life food-limitation and adult reproductive environment. However, little is known about how these parental life stage-specific environments interact with each other and with the offspring environment to influence offspring phenotype, particularly in organisms that realize distinct niches across ontogeny. We examined the effects of parental early life starvation and adult reproductive environment on offspring traits under matching or mismatching offspring early life starvation conditions using the holometabolous, haplo-diploid insect Athalia rosae (turnip sawfly). We show that the parental early life starvation treatment had context-dependent intergenerational effects on the life-history and consumption traits of offspring larvae, partly in interaction with offspring conditions and sex, while there was no significant effect of parental adult reproductive environment. In addition, while offspring larval starvation led to numerous gene- and pathway-level expression differences, parental starvation impacted fewer genes and only the ribosomal pathway. Our findings reveal that parental starvation evokes complex intergenerational effects on offspring life-history traits, consumption patterns as well as gene expression, although the effects are less pronounced than those of offspring starvation.

Eco-evolutionary dynamics of nested Darwinian populations and the emergence of community-level heredity

Interactions among microbial cells can generate new chemistries and functions, but exploitation requires establishment of communities that reliably recapitulate community-level phenotypes. Using mechanistic mathematical models, we show how simple manipulations to population structure can exogenously impose Darwinian-like properties on communities. Such scaffolding causes communities to participate directly in the process of evolution by natural selection and drives the evolution of cell-level interactions to the point where, despite underlying stochasticity, derived communities give rise to offspring communities that faithfully re-establish parental phenotype. The mechanism is akin to a developmental process (developmental correction) that arises from density-dependent interactions among cells. Knowledge of ecological factors affecting evolution of developmental correction has implications for understanding the evolutionary origin of major egalitarian transitions, symbioses, and for top-down engineering of microbial communities.

Proteomic responses to ocean acidification in the brain of juvenile coral reef fish

Elevated CO2 levels predicted to occur by the end of the century can affect the physiology and behaviour of marine fishes. For one important survival mechanism, the response to chemical alarm cues from conspecifics, substantial among-individual variation in the extent of behavioural impairment when exposed to elevated CO2 has been observed in previous studies. Whole brain transcriptomic data has further emphasized the importance of parental phenotypic variation in the response of juvenile fish to elevated CO2. In this study, we investigate the genome-wide proteomic responses of this variation in the brain of 5-week old spiny damselfish, Acanthochromis polyacanthus. We compared the expression of proteins in the brains of juvenile A. polyacanthus from two different parental behavioural phenotypes (sensitive and tolerant) that had been experimentally exposed to short-term, long-term and inter-generational elevated CO2. Our results show differential expression of key proteins related to stress response and epigenetic markers with elevated CO2 exposure. Proteins related to neurological development were also differentially expressed particularly in the long-term developmental treatment, which might be critical for juvenile development. By contrast, exposure to elevated CO2 in the parental generation resulted in only three differentially expressed proteins in the offspring, revealing potential for inter-generational acclimation. Lastly, we found a distinct proteomic pattern in juveniles due to the behavioural sensitivity of parents to elevated CO2, even though the behaviour of the juvenile fish was impaired regardless of parental phenotype. Our data shows that developing juveniles are affected in their brain protein expression by elevated CO2, but the effect varies with the length of exposure as well as due to variation of parental phenotypes in the population.

Vasoactive intestinal peptide as a mediator of the effects of a supergene on social behaviour

Supergenes, or linked groups of alleles that are inherited together, present excellent opportunities to understand gene–behaviour relationships. In white-throated sparrows ( Zonotrichia albicollis ), a supergene on the second chromosome associates with a more aggressive and less parental phenotype. This supergene includes the gene for vasoactive intestinal peptide (VIP), a neuropeptide known to play a causal role in both aggression and parental behaviour. Here, using a free-living population, we compared the levels of VIP mRNA between birds with and without the supergene. We focused on the anterior hypothalamus and infundibular region, two brain regions containing VIP neurons known to play a causal role in aggression and parental behaviour, respectively. First, we show that the supergene enhances VIP expression in the anterior hypothalamus and that expression positively predicts vocal aggression independently of genotype in both sexes. Next, we show that the supergene reduces VIP expression in the infundibular region, which suggests reduced secretion of prolactin, a pro-parental hormone. Thus, the patterns of VIP expression in these two regions are consistent with the enhanced aggression and reduced parental behaviour of birds with the supergene allele. Our results illustrate mechanisms by which elements of genomic architecture, such as supergenes, can contribute to the evolution of alternative behavioural phenotypes.

Universal rules for the interaction of selection and transmission in evolution

The Price equation shows that evolutionary change can be written in terms of two fundamental variables: the fitness of parents (or ancestors) and the phenotypes of their offspring (descendants). Its power lies in the fact that it requires no simplifying assumptions other than a closed population, but realizing the full potential of Price’s result requires that we flesh out the mathematical representation of both fitness and offspring phenotype. Specifically, both need to be treated as stochastic variables that are themselves functions of parental phenotype. Here, I show how new mathematical tools allow us to do this without introducing any simplifying assumptions. Combining this representation of fitness and phenotype with the stochastic Price equation reveals fundamental rules underlying multivariate evolution and the evolution of inheritance. Finally, I show how the change in the entire phenotype distribution of a population, not simply the mean phenotype, can be written as a single compact equation from which the Price equation and related results can be derived as special cases. This article is part of the theme issue ‘Fifty years of the Price equation’.