Testing the evolutionary potential of an alpine plant: phenotypic plasticity in response to growth temperature outweighs parental environmental effects and other genetic causes of variation.

Phenotypic plasticity and rapid evolution are fundamental processes by which organisms can maintain their function and fitness in the face of environmental changes. Here we quantified the plasticity and evolutionary potential of an alpine herb Wahlenbergia ceracea. Utilizing its mixed-mating system, we generated outcrossed and self-pollinated families that were grown in either cool or warm environments, and that had parents that had also been grown in either cool or warm environments. We then analysed the contribution of environmental and genetic factors to variation in a range of phenotypic traits including phenology, leaf mass per area, photosynthetic function, thermal tolerance, and reproductive fitness. The strongest effect was that of current growth temperature, indicating strong phenotypic plasticity. All traits except thermal tolerance were plastic, whereby warm-grown plants flowered earlier, grew larger, and produced more reproductive stems compared with cool-grown plants. Flowering onset and biomass were heritable and under selection, with early flowering and larger plants having higher relative fitness. There was little evidence for transgenerational plasticity, maternal effects, or genotype×environment interactions. Inbreeding delayed flowering and reduced reproductive fitness and biomass. Overall, we found that W. ceracea has the capacity to respond rapidly to climate warming via plasticity, and the potential for evolutionary change.

Negative parental and offspring environmental effects of macroalgae on coral recruitment are linked with alterations in the coral larval microbiome.

The persistence of reef-building corals is threatened by macroalgal competitors leading to a major demographic bottleneck in coral recruitment. Whether parental effects exist under coral-algal competition and whether they influence offspring performance via microbiome alterations represent major gaps in our understanding of the mechanisms by which macroalgae may hinder coral recovery. We investigated the diversity, variability and composition of the microbiome of adults and larvae of the coral Pocillopora acuta and surrounding benthic substrate on algal-removed and algal-dominated bommies. We then assessed the relative influence of parental and offspring environmental effects on coral recruitment processes by reciprocally exposing coral larvae from two parental origins (algal-removed and algal-dominated bommies) to algal-removed and algal-dominated environmental conditions. Dense macroalgal assemblages impacted the microbiome composition of coral larvae. Larvae produced by parents from algal-dominated bommies were depleted in putative beneficial bacteria and enriched in opportunistic taxa. These larvae had a significantly lower survival compared to larvae from algal-removed bommies regardless of environmental conditions. In contrast, algal-induced parental and offspring environmental effects interacted to reduce the survival of coral recruits. Together our results demonstrate negative algal-induced parental and offspring environmental effects on coral recruitment that could be mediated by alterations in the offspring microbiome.

Short-term heat waves have long-term consequences for parents and offspring in stickleback.

Extreme temperature events, such as heat waves, can have lasting effects on the behavior, physiology, and reproductive success of organisms. Here, we examine the impact of short-term exposure to a simulated heat wave on condition, parental care, and reproductive success in a population of threespine stickleback (Gasterosteus aculeatus), a small fish with exclusive paternal care, currently experiencing regular heat waves. Males were either exposed to a simulated heat wave (23 °C) for 5 d or held at an ideal temperature (18 °C). Following this 5-d treatment, all males were transferred to 18 °C, where they completed a full parenting cycle. Offspring were raised at 18 °C. We found that while mass and body condition were unaffected in males exposed to a heat wave, cortisol responses were dampened across the nesting cycle compared to control males. In addition, heat wave males had longer latency for eggs to hatch, lower hatching success, and showed lower levels of parental care behavior compared to control males. Offspring of heat wave males had lower body condition, affecting swimming performance. Altogether, our results highlight the long-term impact that even short-term events can have on reproductive success, parental behavior, and subsequent generations, providing insight into population responses to rapid environmental change.

Noise pollution causes parental stress on marine invertebrates, the Giant scallop example.

In marine invertebrates, abiotic stresses on adults can act directly on gametes quality, which impacts phenotype and development success of the offspring. Human activities introduce noise pollution in the marine environment but still few studies on invertebrates have considered the impacts on adult or larval stages separately, and to our knowledge, never investigated the cross-generational effects of anthropogenic noise. This article explores parental effects of pile driving noise associated with the building phase of offshore wind turbines on a coastal invertebrate, Pecten maximus (L.). Adults were exposed to increasing levels of sound during gametogenesis, then their offspring were also exposed. The results highlight that anthropogenic noise experienced by the parents reduces their reproductive investment and modify larval response in similar conditions. Also, larvae from exposed adults grew 6-fold faster and metamorphosed 5-fold faster, which could be an amplified adaptive strategy to reduce the pelagic phase in a stressful environment.

Parental exposure to antidepressants has lasting effects on offspring? A case study with zebrafish.

Fish have common neurotransmitter pathways with humans, exhibiting a significant degree of conservation and homology. Thus, exposure to fluoxetine makes fish potentially susceptible to biochemical and physiological changes, similarly to what is observed in humans. Over the years, several studies demonstrated the potential effects of fluoxetine on different fish species and at different levels of biological organization. However, the effects of parental exposure to unexposed offspring remain largely unknown. The consequences of 15-day parental exposure to relevant concentrations of fluoxetine (100 and 1000 ng/L) were assessed on offspring using zebrafish as a model organism. Parental exposure resulted in offspring early hatching, non-inflation of the swimming bladder, increased malformation frequency, decreased heart rate and blood flow, and reduced growth. Additionally, a significant behavioral impairment was also found (reduced startle response, basal locomotor activity, and altered non-associative learning during early stages and a negative geotaxis and scototaxis, reduced thigmotaxis, and anti-social behavior at later life stages). These behavior alterations are consistent with decreased anxiety, a significant increase in the expression of the monoaminergic genes slc6a4a (sert), slc6a3 (dat), slc18a2 (vmat2), mao, tph1a, and th2, and altered levels of monoaminergic neurotransmitters. Alterations in behavior, expression of monoaminergic genes, and neurotransmitter levels persisted until offspring adulthood. Given the high conservation of neuronal pathways between fish and humans, data show the possibility of potential transgenerational and multigenerational effects of pharmaceuticals' exposure. These results reinforce the need for transgenerational and multigenerational studies in fish, under realistic scenarios, to provide realistic insights into the impact of these pharmaceuticals.

Genetic relatedness can alter the strength of plant-soil interactions.

PREMISE: Intraspecific variation may play a key role in shaping the relationships between plants and their interactions with soil microbial communities. The soil microbes of individual plants can generate intraspecific variation in the responsiveness of the plant offspring, yet have been much less studied. To address this need, we explored how the relatedness of seedlings from established clones of Solidago altissima altered the plant-soil interactions of the seedlings. METHODS: Seedlings of known parentage were generated from a series of 24 clones grown in a common garden. Seedlings from these crosses were inoculated with soils from maternal, paternal, or unrelated clones and their performance compared to sterilized control inocula. RESULTS: We found that soil inocula influenced by S. altissima clones had an overall negative effect on seedling biomass. Furthermore, seedlings inoculated with maternal or paternal soils tended to experience larger negative effects than seedlings inoculated with unrelated soils. However, there was much variation among individual crosses, with not all responding to relatedness. CONCLUSIONS: Our data argue that genetic relatedness to the plant from which the soil microbial inoculum was obtained may cause differential impacts on establishing seedlings, encouraging the regeneration of non-kin adjacent to established clones. Such intraspecific variation represents a potentially important source of heterogeneity in plant-soil microbe interactions with implications for maintaining population genetic diversity.

The impact of parental and developmental stress on DNA methylation in the avian hypothalamic-pituitary-adrenal axis.

The hypothalamic-pituitary-adrenal (HPA) axis coordinates an organism's response to environmental stress. The responsiveness and sensitivity of an offspring's stress response may be shaped not only by stressors encountered in their early post-natal environment but also by stressors in their parent's environment. Yet, few studies have considered how stressors encountered in both of these early life environments may function together to impact the developing HPA axis. Here, we manipulated stressors in the parental and post-natal environments in a population of house sparrows (Passer domesticus) to assess their impact on changes in DNA methylation (and corresponding gene expression) in a suite of genes within the HPA axis. We found that nestlings that experienced early life stress across both life-history periods had higher DNA methylation in a critical HPA axis gene, the glucocorticoid receptor (NR3C1). In addition, we found that the life-history stage when stress was encountered impacted some genes (HSD11B1, NR3C1 and NR3C2) differently. We also found evidence for the mitigation of parental stress by post-natal stress (in HSD11B1 and NR3C2). Finally, by assessing DNA methylation in both the brain and blood, we were able to evaluate cross-tissue patterns. While some differentially methylated regions were tissue-specific, we found cross-tissue changes in NR3C2 and NR3C1, suggesting that blood is a suitable tissue for assessing DNA methylation as a biomarker of early life stress. Our results provide a crucial first step in understanding the mechanisms by which early life stress in different life-history periods contributes to changes in the epigenome of the HPA axis.

Parental early life environments drive transgenerational plasticity of offspring metabolism in a freshwater fish (Danio rerio).

Parental experiences can lead to changes in offspring phenotypes through transgenerational plasticity (TGP). TGP is expected to play a role in improving the responses of offspring to changes in climate, but little is known about how the early lives of parents influence offspring TGP. Here, we use a model organism, zebrafish (Danio rerio), to contrast the effects of early and later life parental thermal environments on offspring routine metabolism. To accomplish this, we exposed both parents to either constant optimal (27°C) or environmentally realistic diel fluctuating (22-32°C) temperatures during early (embryonic and larval) and later (juvenile and adult) life in a factorial design. We found significant reduction of routine metabolic rates (greater than 20%) at stressful temperatures (22°C and 32°C) after biparental early life exposure to fluctuating temperatures, but little effect of later life parental temperatures on offspring metabolism. This reduction reflects metabolic compensation and is expected to enhance offspring body sizes under stressful temperatures. These changes occur over and above the effects of parental environments on egg size, suggesting alternate non-genetic mechanisms influenced offspring metabolic rates.

Rapid decline of prenatal maternal effects with age is independent of postnatal environment in a precocial bird.

Maternal effects are an important source of phenotypic variation with potentially large fitness consequences, but how their importance varies with the quality of the environment across an individual's ontogeny is poorly understood. We bred Japanese quail (Coturnix japonica) of known pedigree and experimentally manipulated the quality of the offspring diet, to estimate the importance of prenatal maternal effects in shaping variation in body mass from hatching to adulthood. Maternal genetic effects on body mass at hatching were strong, and largely caused by variation in egg mass, but their importance rapidly declined with age. Whereas there was a large effect of diet on growth, this did not affect the decline of maternal effects variance. The importance of additive genetic and residual variance increased with age, with the latter being considerably larger in the poor diet treatment. Hence, we found no evidence for prenatal maternal effect by postnatal environment interactions and that prenatal maternal effects are rapidly replaced by direct additive genetic and residual effects when offspring start to develop outside the egg. Thereby these results shed new light on the dynamics of the role of maternal versus offspring genes across ontogeny and environments.

Differential effects of parental and developmental temperatures on larval thermal adaptation in oviparous and viviparous model fish species.

Phenotypic plasticity has been identified as a major mechanism of response to changing temperatures. Parental effects are potentially important drivers of ecological and evolutionary dynamics, while developmental plasticity also plays a key role in generating phenotypic variation. However, little is known of the interaction between parental effects and developmental plasticity on the thermal phenotypes of fishes with different reproductive modes (i.e. oviparous vs. viviparous). To understand the contributions of inter- and intra-generational plasticity of thermal phenotypes (preferred temperature, avoidance temperatures, critical thermal thresholds) in fishes with different reproductive modes, we carried out a factorial experiment in which both breeding parents and offspring were exposed to lower (22 °C) or higher (28 °C) temperatures, using zebrafish (Danio rerio) and guppies (Poecilia reticulata) as representative oviparous and viviparous species. We found that offspring thermal preference and avoidance of both species were significantly influenced by parental effects and developmental plasticity, with higher thermal preference and avoidance consistent with higher background (parental) temperature treatments. However, parental effects were only found to impose significant effect on the thermal tolerances of guppies. The findings suggest that phenotypic plasticity, both within and across generations, may be an important mechanism to adapt to rapid climate changes, and that future temperature fluctuations may impose more profound effects on viviparous fish species in general.

Variation in Embryonic Metabolic Reaction Norms and the Role of the Environment.

AbstractEarly developmental environments can shape how organisms respond to later environments, but despite the potential for this phenomenon to alter the evolution of phenotypes and their underlying mechanisms in variable environments, details of this process are not understood. For example, both temperature and parental age can alter offspring metabolic plasticity and growth within species, yet the extent of such effects is unknown. We measured the reaction norms of embryonic heart rate in response to egg temperature and the change in egg mass over the incubation period in wild house sparrows. Using Bayesian linear mixed models, we estimated covariation in the intercepts and slopes of these reaction norms among clutches and eggs. We found that heart rate intercepts, not slopes, varied among clutches and that neither intercepts nor slopes varied among eggs within clutches. In contrast, egg mass intercepts and slopes varied among clutches and eggs. Ambient temperature did not explain variance in reaction norms. Instead, individuals from older mothers were more metabolically sensitive to egg temperature and lost less mass over the incubation period than individuals from younger mothers. Nevertheless, heart rate reaction norms and egg mass reaction norms did not covary. Our results suggest that early environments influenced by parents may contribute to variation in embryonic reaction norms. The structure of variation in embryonic reaction norms that exists both among clutches and among eggs demonstrates a complexity in plastic phenotypes that should be explored in future work. Furthermore, the potential for the embryonic environment to shape the reaction norms of other traits has implications for the evolution of plasticity more broadly.

From mechanism to ecosystem: building bridges between ecoimmunology, psychoneuroimmunology and disease ecology.

Historically, the fields of ecoimmunology, psychoneuroimmunology and disease ecology have taken complementary yet disparate theoretical and experimental approaches, despite sharing critical common themes. Researchers in these areas have largely worked independently of one another to understand mechanistic immunological responses, organismal level immune performance, behavioral changes, and host and parasite/disease population dynamics, with few bridges across disciplines. Although efforts to strengthen and expand these bridges have been called for (and occasionally heeded) over the last decade, more integrative studies are only now beginning to emerge, with critical gaps remaining. Here, we briefly discuss the origins of these key fields, and their current state of integration, while highlighting several critical directions that we suggest will strengthen their connections into the future. Specifically, we highlight three key research areas that provide collaborative opportunities for integrative investigation across multiple levels of biological organization, from mechanisms to ecosystems: (1) parental effects of immunity, (2) microbiome and immune function and (3) sickness behaviors. By building new bridges among these fields, and strengthening existing ones, a truly integrative approach to understanding the role of host immunity on individual and community fitness is within our grasp.

Sex-specific transgenerational plasticity: developmental temperatures of mothers and fathers have different effects on sons and daughters.

Each parent can influence offspring phenotype via provisioning of the zygote or sex-specific DNA methylation. Transgenerational plasticity may therefore depend on the environmental conditions experienced by each parent. We tested this hypothesis by conducting a fully factorial experiment across three generations of guppies (Poecilia reticulata), determining the effects of warm (28°C) and cold (21°C) thermal backgrounds of mothers and fathers on mass and length, and thermal performance (sustained and sprint swimming speeds, citrate synthase and lactate dehydrogenase activities; 18, 24, 28, 32 and 36°C test temperatures) of sons and daughters. Offspring sex was significant for all traits except for sprint speed. Warmer mothers produced sons and daughters with reduced mass and length, and warmer fathers produced shorter sons. Sustained swimming speed (Ucrit) of male offspring was greatest when both parents were raised at 28°C, and warmer fathers produced daughters with greater Ucrit. Similarly, warmer fathers produced sons and daughters with greater metabolic capacity. We show that the thermal variation experienced by parents can modify offspring phenotype, and that predicting the impacts of environmental change on populations would require knowledge of the thermal background of each mother and father, particularly where sexes are spatially segregated.

Transgenerational effects on body size and survival in Brook charr (Salvelinus fontinalis).

Higher temperatures are now observed in several ecosystems and act as new selective agents that shape traits and fitness of individuals. Transgenerational effects may be important in modulating adaptation of future generations and buffering negative impacts of temperature changes. The potential for these effects may be important in freshwater fish species, as temperature is a key abiotic component of their environment. Yet, still, relatively few studies have assessed the presence and importance of transgenerational effects under natural conditions. The purpose of this study was to test how parental thermal conditions influenced offspring growth and survival following stocking in Brook charr (Salvelinus fontinalis). To do so, part of the breeders were exposed to a "cold" treatment while others were exposed to a "warm" treatment during the final steps of gonad maturation (constant 2°C difference between treatments along the seasonal temperature decrease). The impact on offspring of a selection treatment targeting production traits of interest (absence of sexual maturation at 1+, combined with increased growth) in breeders was also evaluated. After 7-8 months of growth in captivity, offspring were stocked in natural lakes. Their growth and survival were assessed about a year later. Offspring from "cold" breeders showed lower survival than those from "warm" breeders and the selection treatment had no effect on survival. However, the selection treatment was linked to lower Fulton's condition index, which, in turn, was positively correlated to survival in lakes. This study highlights the importance of working in ecological/industrial context to fully assess the different impacts of transgenerational effects on traits and survival. Our results also have important implications for stocking practices used to support the sport fishing industry.

Variable ambient temperature promotes song learning and production in zebra finches.

Current climate change is leading to increasingly unpredictable environmental conditions and is imposing new challenges to wildlife. For example, ambient conditions fluctuating during critical developmental periods could potentially impair the development of cognitive systems and may therefore have a long-term influence on an individual's life. We studied the impact of temperature variability on zebra finch cognition, focusing on song learning and song quality (N = 76 males). We used a 2 × 2 factorial experiment with two temperature conditions (stable and variable). Half of the juveniles were cross-fostered at hatching to create a mismatch between pre- and posthatching conditions, the latter matching this species' critical period for song learning. We found that temperature variability did not affect repertoire size, syllable consistency, or the proportion of syllables copied from a tutor. However, birds that experienced variable temperatures in their posthatching environment were more likely to sing during recordings. In addition, birds that experienced variable prenatal conditions had higher learning accuracy than birds in stable prenatal environments. These findings are the first documented evidence that variable ambient temperatures can influence song learning in zebra finches. Moreover, they indicate that temperature variability can act as a form of environmental enrichment with net positive effects on cognition.

Trans-generational immune priming is not mediated by the sex of the parent primed: a meta-analysis of invertebrate data.

Traditionally, only vertebrates were thought capable of acquired immune responses, such as the ability to transfer immunological experience vertically to their offspring (known as trans-generational immune priming, TGIP). Increasing evidence challenges this belief and it is now clear that invertebrates also have the ability to exhibit functionally equivalent TGIP. This has led to a surge in papers exploring invertebrate TGIP, with most focusing on the costs, benefits or factors that affect the evolution of this trait. Whilst many studies have found support for the phenomenon, not all studies do, and there is considerable variation in the strength of positive results. To address this, we conducted a meta-analysis to answer the question: what is the overall effect of TGIP in invertebrates? Then, to understand the specific factors that affect its presence and intensity, we conducted a moderator analysis. Our results corroborate that TGIP occurs in invertebrates (demonstrated by a large, positive effect size). The strength of the positive effect was related to if and how offspring were immune challenged (i.e. whether they were challenged with the same or different insult as their parents or not challenged at all). Interestingly, there was no effect of the ecology or life history of the species or the sex of the parent or the offspring primed, and responses were comparable across different immune elicitors. Our publication bias testing suggests that the literature may suffer from some level of positive-result bias. However, even after accounting for potential bias, our effect size remains positive. Publication bias testing can be influenced by diversity in the data set, which was considerable in our data, even after moderator analysis. It is therefore conceivable that differences among studies could be caused by other moderators that were unable to be included in our meta-analysis. Nonetheless, our results suggest that TGIP does occur in invertebrates, whilst providing some potential avenues to examine the factors that account for variation in effect sizes.

Preterm birth and educational disadvantage: Heterogeneous effects.

Although preterm birth is the leading cause of perinatal morbidity and mortality in advanced economies, evidence about the consequences of prematurity in later life is limited. Using Swedish registers for cohorts born 1982-94 (N  =  1,087,750), we examine the effects of preterm birth on school grades at age 16 using sibling fixed effects models. We further examine how school grades are affected by degree of prematurity and the compensating roles of family socio-economic resources and characteristics of school districts. Our results show that the negative effects of preterm birth are observed mostly among children born extremely preterm (<28 weeks); children born moderately preterm (32-<37 weeks) suffer no ill effects. We do not find any evidence for a moderating effect of parental socio-economic resources. Children born extremely preterm and in the top decile of school districts achieve as good grades as children born at full term in an average school district.Supplementary material for this article is available at: http://dx.doi.org/10.1080/00324728.2022.2080247.

The estimation of environmental and genetic parental influences.

Parents share half of their genes with their children, but they also share background social factors and actively help shape their child's environment - making it difficult to disentangle genetic and environmental causes of parent-offspring similarity. While adoption and extended twin family designs have been extremely useful for distinguishing genetic and nongenetic parental influences, these designs entail stringent assumptions about phenotypic similarity between relatives and require samples that are difficult to collect and therefore are typically small and not publicly shared. Here, we describe these traditional designs, as well as modern approaches that use large, publicly available genome-wide data sets to estimate parental effects. We focus in particular on an approach we recently developed, structural equation modeling (SEM)-polygenic score (PGS), that instantiates the logic of modern PGS-based methods within the flexible SEM framework used in traditional designs. Genetically informative designs such as SEM-PGS rely on different and, in some cases, less rigid assumptions than traditional approaches; thus, they allow researchers to capitalize on new data sources and answer questions that could not previously be investigated. We believe that SEM-PGS and similar approaches can lead to improved insight into how nature and nurture combine to create the incredible diversity underlying human behavior.

Inbreeding effects on telomeres in hatchling sand lizards (Lacerta agilis): An optimal family affair?

Telomeres are nucleotide-protein caps, predominantly at the ends of Metazoan linear chromosomes, showing complex dynamics with regard to their lengthening and shortening through life. Their complexity has entertained the idea that net telomere length and attrition could be valuable biomarkers of phenotypic and genetic quality of their bearer. Intuitively, those individuals could be more heterozygous and, hence, less inbred. However, some inbred taxa have longer, not shorter, telomeres. To understand the role of inbreeding in this complex scenario we need large samples across a range of genotypes with known maternity and paternity in telomere-screened organisms under natural conditions. We assessed the effects of parental and hatchling inbreeding on telomere length in >1300 offspring from >500 sires and dams in a population of sand lizards (Lacerta agilis). Maternal and paternal ID and their interactions predict hatchling telomere length at substantial effect sizes (R2  > .50). Deviation from mean maternal heterozygosity statistically predicts shorter offspring telomeres but this only when sibship is controlled for by paternal ID, and then is still limited (R2  = .06). Raw maternal heterozygosity scores, ignoring absolute deviation from the mean, explained 0.07% of the variance in hatchling telomere length. In conclusion, inbreeding is not a driver of telomere dynamics in the sand lizard (Lacerta agilis) study system.

Parental methylation mediates how progeny respond to environments of parents and of progeny themselves.

BACKGROUND AND AIMS: Environments experienced by both parents and offspring influence progeny traits, but the epigenetic mechanisms that regulate the balance of parental vs. progeny control of progeny phenotypes are not known. We tested whether DNA methylation in parents and/or progeny mediates responses to environmental cues experienced in both generations. METHODS: Using Arabidopsis thaliana, we manipulated parental and progeny DNA methylation both chemically, via 5-azacytidine, and genetically, via mutants of methyltransferase genes, then measured progeny germination responses to simulated canopy shade in parental and progeny generations. KEY RESULTS: We first found that germination of offspring responded to parental but not seed demethylation. We further found that parental demethylation reversed the parental effect of canopy in seeds with low (Cvi-1) to intermediate (Col) dormancy, but it obliterated the parental effect in seeds with high dormancy (Cvi-0). Demethylation did so by either suppressing germination of seeds matured under white-light (Cvi-1) or under canopy (Cvi-0), or by increasing the germination of seeds matured under canopy (Col). Disruption of parental methylation also prevented seeds from responding to their own light environment in one genotype (Cvi-0, most dormant), but it enabled seeds to respond to their own environment in another genotype (Cvi-1, least dormant). Using mutant genotypes, we found that both CG and non-CG DNA methylation were involved in parental effects on seed germination. CONCLUSIONS: Parental methylation state influences seed germination more strongly than does the progeny's own methylation state, and it influences how seeds respond to environments of parents and progeny in a genotype-specific manner.