Cardiac physiology and metabolic gene expression during late organogenesis among F. heteroclitus embryo families from crosses between pollution-sensitive and -resistant parents

Background The teleost fish Fundulus heteroclitus inhabit estuaries heavily polluted with persistent and bioaccumulative chemicals. While embryos of parents from polluted sites are remarkably resistant to toxic sediment and develop normally, embryos of parents from relatively clean estuaries, when treated with polluted sediment extracts, are developmentally delayed, displaying deformities characteristic of pollution-induced embryotoxicity. To gain insight into parental effects on sensitive and resistant phenotypes during late organogenesis, we established sensitive, resistant, and crossed embryo families using five female and five male parents from relatively clean and predominantly PAH-polluted estuaries each, measured heart rates, and quantified individual embryo expression of 179 metabolic genes. Results Pollution-induced embryotoxicity manifested as morphological deformities, significant developmental delays, and altered cardiac physiology was evident among sensitive embryos resulting from crosses between females and males from relatively clean estuaries. Significantly different heart rates among several geographically unrelated populations of sensitive, resistant, and crossed embryo families during late organogenesis and pre-hatching suggest site-specific adaptive cardiac physiology phenotypes relative to pollution exposure. Metabolic gene expression patterns (32 genes, 17.9%, at p < 0.05; 11 genes, 6.1%, at p < 0.01) among the embryo families indicate maternal pollutant deposition in the eggs and parental effects on gene expression and metabolic alterations. Conclusion Heart rate differences among sensitive, resistant, and crossed embryos is a reliable phenotype for further explorations of adaptive mechanisms. While metabolic gene expression patterns among embryo families are suggestive of parental effects on several differentially expressed genes, a definitive adaptive signature and metabolic cost of resistant phenotypes is unclear and shows unexpected sensitive-resistant crossed embryo expression profiles. Our study highlights physiological and metabolic gene expression differences during a critical embryonic stage among pollution sensitive, resistant, and crossed embryo families, which may contribute to underlying resistance mechanisms observed in natural F. heteroclitus populations living in heavily contaminated estuaries.

Lipid-Associated Variants near ANGPTL3 and LPL Show Parent-of-Origin Specific Effects on Blood Lipid Levels and Obesity

Parent-of-origin effects (POE) and sex-specific parental effects have been reported for plasma lipid levels, and a strong relationship exists between dyslipidemia and obesity. We aim to explore whether genetic variants previously reported to have an association to lipid traits also show POE on blood lipid levels and obesity. Families from the Botnia cohort and the Hungarian Transdanubian Biobank (HTB) were genotyped for 12 SNPs, parental origin of alleles were inferred, and generalized estimating equations were modeled to assess parental-specific associations with lipid traits and obesity. POE were observed for the variants at the TMEM57, DOCK7/ANGPTL3, LPL, and APOA on lipid traits, the latter replicated in HTB. Sex-specific parental effects were also observed; variants at ANGPTL3/DOCK7 showed POE on lipid traits and obesity in daughters only, while those at LPL and TMEM57 showed POE on lipid traits in sons. Variants at LPL and DOCK7/ANGPTL3 showed POE on obesity-related traits in Botnia and HTB, and POE effects on obesity were seen to a higher degree in daughters. This highlights the need to include analysis of POEs in genetic studies of complex traits.

Parental environmental effects are common and strong, but unpredictable, in Arabidopsis thaliana

The phenotypes of plants can be influenced by the environmental conditions experienced by their parents. In some cases, such parental effects have been found to be adaptive, which has led to much speculation about their ecological and evolutionary significance. However, there is still much uncertainty about how common and how predictable parental environmental effects really are. We carried out a comprehensive test for parental effects of different environmental stresses in the model plant Arabidopsis thaliana. We subjected plants of three Arabidopsis genotypes to a broad range of biotic or abiotic stresses, or combinations thereof, and compared their offspring phenotypes in a common environment. The majority of environmental stresses (16 out of 24 stress treatments) caused significant parental effects, in particular on plant biomass and reproduction, with positive or negative effects ranging from 35% to +38% changes in offspring fitness. The expression of parental effects was strongly genotype-dependent, with some effects only present in some genotypes but absent, or even in the opposite direction, in others. Parental effects of multiple environmental stresses were often non-additive, and their effects can thus not be predicted from what we know about the effects of individual stresses. Intriguingly, the direction and magnitude of parental effects were unrelated to the direct effects on the parents: some stresses did not affect the parents but caused substantial effects on offspring, while for others the situation was reversed. In summary, parental environmental effects are common and often strong in A. thaliana, but they are genotype-dependent and difficult to predict.

Predator-induced maternal effects determine adaptive antipredator behaviors via egg composition

In high-risk environments with frequent predator encounters, efficient antipredator behavior is key to survival. Parental effects are a powerful mechanism to prepare offspring for coping with such environments, yet clear evidence for adaptive parental effects on offspring antipredator behaviors is missing. Rapid escape reflexes, or “C-start reflexes,” are a key adaptation in fish and amphibians to escape predator strikes. We hypothesized that mothers living in high-risk environments might induce faster C-start reflexes in offspring by modifying egg composition. Here, we show that offspring of the cichlid fish Neolamprologus pulcher developed faster C-start reflexes and were more risk averse if their parents had been exposed to cues of their most dangerous natural predator during egg production. This effect was mediated by differences in egg composition. Eggs of predator-exposed mothers were heavier with higher net protein content, and the resulting offspring were heavier and had lower igf-1 gene expression than control offspring shortly after hatching. Thus, changes in egg composition can relay multiple putative pathways by which mothers can influence adaptive antipredator behaviors such as faster escape reflexes.

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.

Depth-dependent parental effects create invisible barriers to coral dispersal

Historically, marine populations were considered to be interconnected across large geographic regions due to the lack of apparent physical barriers to dispersal, coupled with a potentially widely dispersive pelagic larval stage. Recent studies, however, are providing increasing evidence of small-scale genetic segregation of populations across habitats and depths, separated in some cases by only a few dozen meters. Here, we performed a series of ex-situ and in-situ experiments using coral larvae of three brooding species from contrasting shallow- and deep-water reef habitats, and show that their settlement success, habitat choices, and subsequent survival are substantially influenced by parental effects in a habitat-dependent manner. Generally, larvae originating from deep-water corals, which experience less variable conditions, expressed more specific responses than shallow-water larvae, with a higher settlement success in simulated parental-habitat conditions. Survival of juvenile corals experimentally translocated to the sea was significantly lower when not at parental depths. We conclude that local adaptations and parental effects alongside larval selectivity and phenotype-environment mismatches combine to create invisible semipermeable barriers to coral dispersal and connectivity, leading to habitat-dependent population segregation.

Plasticity in parental effects confers rapid larval thermal tolerance in the estuarine anemone Nematostella vectensis

ABSTRACTParental effects can prepare offspring for different environments and facilitate survival across generations. We exposed parental populations of the estuarine anemone, Nematostella vectensis, from Massachusetts to elevated temperatures and quantified larval mortality across a temperature gradient. We found that parental exposure to elevated temperatures resulted in a consistent increase in larval thermal tolerance, as measured by the temperature at which 50% of larvae die (LT50), with a mean increase in LT50 of 0.3°C. Larvae from subsequent spawns returned to baseline thermal thresholds when parents were returned to normal temperatures, indicating plasticity in these parental effects. Histological analyses of gametogenesis in females suggested that these dynamic shifts in larval thermal tolerance may be facilitated by maternal effects in non-overlapping gametic cohorts. We also compared larvae from North Carolina (a genetically distinct population with higher baseline thermal tolerance) and Massachusetts parents, and observed that larvae from heat-exposed Massachusetts parents had thermal thresholds comparable to those of larvae from unexposed North Carolina parents. North Carolina parents also increased larval thermal tolerance under the same high-temperature regime, suggesting that plasticity in parental effects is an inherent trait for N. vectensis. Overall, we find that larval thermal tolerance in N. vectensis shows a strong genetic basis and can be modulated by parental effects. Further understanding of the mechanisms behind these shifts can elucidate the fate of thermally sensitive ectotherms in a rapidly changing thermal environment.

Indirect parental effects on offspring viability by egg-derived fluids in an external fertilizer

The capacity for parents to influence offspring phenotypes via nongenetic inheritance is currently a major area of focus in evolutionary biology. Intriguing recent evidence suggests that sexual interactions among males and females, both before and during mating, are important mediators of such effects. Sexual interactions typically extend beyond gamete release, involving both sperm and eggs, and their associated fluids. However, the potential for gamete-level interactions to induce nongenetic parental effects remains under-investigated. Here, we test for such effects using an emerging model system for studying gamete interactions, the external fertilizer Mytilus galloprovincialis . We employed a split-ejaculate design to test whether exposing sperm to egg-derived chemicals (ECs) from a female would affect fertilization rate and offspring viability when those sperm were used to fertilize a different female's eggs. We found separate, significant effects of ECs from non-fertilizing females on both fertilization rate and offspring viability. The offspring viability effect indicates that EC-driven interactions can have nongenetic implications for offspring fitness independent of the genotypes inherited by those offspring. These findings provide a rare test of indirect parental effects driven exclusively by gamete-level interactions, and to our knowledge the first evidence that such effects occur via the gametic fluids of females.