An official website of the United States government
It is well established that environmental signals can induce phenotypic responses that persist for multiple generations. The induction of such ‘transgenerational plasticity’ (TGP) depends upon the ability of organisms to accurately receive and process information from environmental signals. Thus, sensory systems are likely intertwined with TGP. Here we tested the link between an environmental stressor and transgenerational responses in a component of the sensory system (eye size) that is linked to enhanced vision and ecologically relevant behaviours. We reared 45 clones of Daphnia pulicaria in the presence and absence of a low-quality resource (cyanobacteria) and evaluated shifts in relative eye size in offspring. Our results revealed divergent shifts in relative eye size within- and across-generations. Parental Daphnia that were fed cyanobacteria produced a smaller eye than Daphnia fed high-quality algae. Such differences were then reversed in the offspring generation; Daphnia whose mothers were fed cyanobacteria produced larger eyes than Daphnia that were continually fed green algae. We discuss the extent to which this maternal effect on eye size is an adaptive response linked to improved foraging.
more »
« less
This content will become publicly available on March 11, 2026
The Transcriptional Landscape of Adaptive Thermal Plasticity Within and Across Generations: The Role of Gene Expression and Alternative Splicing
ABSTRACT There is increasing evidence for the co‐occurrence of adaptive within‐generation (WGP) and transgenerational (TGP) plasticity and the ecological scenarios driving both types of plasticity. However, some aspects of their transcriptional mechanisms, such as the role of alternative splicing and the consequences of parental acclimation across life stages, have remained elusive. We explore these fundamental questions by considering the desert endemicDrosophila mojavensisfor which prior evidence indicates adaptive thermal acclimation within and across generations. We implement a full factorial design to estimate genome‐wide patterns of differential gene expression (DE) and alternative splicing (AS) in response to acclimation treatments performed in the parental and offspring generations, as well as considering larval and adult stages. Our results demonstrate that mechanisms of alternative splicing represent a substantial difference between WGP and TGP. These mechanisms contribute substantially to transcriptional plasticity within generations but not across generations. We found a great number of genes associated with transcriptional TGP, which is exclusive to larval stages and not adult samples. Finally, we provide evidence demonstrating opposing transcriptional trajectories in differential gene expression between WGP and TGP. Thus, parental acclimation appears to up‐regulate genes that are down‐regulated during offspring acclimation. This pattern suggests a possible hypothesis for the mechanisms explaining the compensatory effect of parental acclimation in the offspring generation.
more »
« less
- Award ID(s):
- 2220279
- PAR ID:
- 10576943
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Molecular Ecology
- Volume:
- 34
- Issue:
- 7
- ISSN:
- 0962-1083
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Begun, D (Ed.)Abstract Changes in gene regulation at multiple levels may comprise an important share of the molecular changes underlying adaptive evolution in nature. However, few studies have assayed within- and between-population variation in gene regulatory traits at a transcriptomic scale, and therefore inferences about the characteristics of adaptive regulatory changes have been elusive. Here, we assess quantitative trait differentiation in gene expression levels and alternative splicing (intron usage) between three closely related pairs of natural populations of Drosophila melanogaster from contrasting thermal environments that reflect three separate instances of cold tolerance evolution. The cold-adapted populations were known to show population genetic evidence for parallel evolution at the SNP level, and here we find evidence for parallel expression evolution between them, with stronger parallelism at larval and adult stages than for pupae. We also implement a flexible method to estimate cis- vs trans-encoded contributions to expression or splicing differences at the adult stage. The apparent contributions of cis- vs trans-regulation to adaptive evolution vary substantially among population pairs. While two of three population pairs show a greater enrichment of cis-regulatory differences among adaptation candidates, trans-regulatory differences are more likely to be implicated in parallel expression changes between population pairs. Genes with significant cis-effects are enriched for signals of elevated genetic differentiation between cold- and warm-adapted populations, suggesting that they are potential targets of local adaptation. These findings expand our knowledge of adaptive gene regulatory evolution and our ability to make inferences about this important and widespread process.more » « less
-
Regulation of gene expression is a critical link between genotype and phenotype explaining substantial heritable variation within species. However, we are only beginning to understand the ways that specific gene regulatory mechanisms contribute to adaptive divergence of populations. In plants, the post-transcriptional regulatory mechanism of alternative splicing (AS) plays an important role in both development and abiotic stress response, making it a compelling potential target of natural selection. AS allows organisms to generate multiple different transcripts/proteins from a single gene and thus may provide a source of evolutionary novelty. Here, we examine whether variation in alternative splicing and gene expression levels might contribute to adaptation and incipient speciation of dune-adapted prairie sunflowers in Great Sand Dunes National Park, Colorado, USA. We conducted a common garden experiment to assess transcriptomic variation among ecotypes and analyzed differential expression, differential splicing, and gene coexpression. We show that individual genes are strongly differentiated for both transcript level and alternative isoform proportions, even when grown in a common environment, and that gene coexpression networks are disrupted between ecotypes. Furthermore, we examined how genome-wide patterns of sequence divergence correspond to divergence in transcript levels and isoform proportions and find evidence for both cis and trans-regulation. Together, our results emphasize that alternative splicing has been an underappreciated mechanism providing source material for natural selection at short evolutionary time scales.more » « less
-
Kelp forests of the California Current System have experienced prolonged marine heatwave (MHW) events that overlap in time with the phenology of life history events (e.g., gametogenesis and spawning) of many benthic marine invertebrates. To study the effect of thermal stress from MHWs during gametogenesis in the purple sea urchin ( Strongylocentrotus purpuratus ) and further, whether MHWs might induce transgenerational plasticity (TGP) in thermal tolerance of progeny, adult urchins were acclimated to two conditions in the laboratory – a MHW temperature of 18°C and a non-MHW temperature of 13°C. Following a four-month long acclimation period (October–January), adults were spawned and offspring from each parental condition were reared at MHW (18°C) and non-MHW temperatures (13°C), creating a total of four embryo treatment groups. To assess transgenerational effects for each of the four groups, we measured thermal tolerance of hatched blastula embryos in acute thermal tolerance trials. Embryos from MHW-acclimated females were more thermally tolerant with higher LT 50 values as compared to progeny from non-MHW-acclimated females. Additionally, there was an effect of female acclimation state on offspring body size at two stages of embryonic development - early gastrulae and prism, an early stage echinopluteus larvae. To assess maternal provisioning as means to also alter embryo performance, we assessed gamete traits from the differentially acclimated females, by measuring size and biochemical composition of eggs. MHW-acclimated females had eggs with higher protein concentrations, while egg size and lipid content showed no differences. Our results indicate that TGP plays a role in altering the performance of progeny as a function of the thermal history of the female, especially when thermal stress coincides with gametogenesis. In addition, the data on egg provisioning show that maternal experience can influence embryo traits via egg protein content. Although this is a laboratory-based study, the results suggest that TGP may play a role in the resistance and tolerance of S. purpuratus early stages in the natural kelp forest setting.more » « less
-
Abstract Parental exposure to environmental stress can influence phenotypic plasticity by offspring developing under that stressor. Transgenerational effects may also reshape natural selection on developmental plasticity by influencing its fitness consequences and expression of its genetic variation. We tested these hypotheses in the purple sea urchinStrongylocentrotus purpuratus, an invertebrate exposed to coastal upwelling (periods of low temperature and pH impacting biomineralization and performance). We conditioned parents and larvae to experimental upwelling and integrated RNA-seq, phenotyping of body size and biomineralization, and measured fitness-correlated traits in a quantitative genetic experiment. Larvae developing under upwelling induced widespread differential expression (DE), decreased biomineralization, and reduced body size. We detected fitness benefits for increased biomineralization and reduced size under upwelling indicative of adaptive plasticity, but only when larvae were spawned from parents exposed to upwelling. Larval DE was largely associated with adaptive phenotypic plasticity. Negative genetic correlation in DE was abundant between genes associated with adaptive plasticity. However, genetic correlations in DE associated with body size plasticity were significantly more positive in larvae from upwelling-exposed parents. These results show that transgenerational effects modify the fitness landscape and genetic architecture of phenotypic plasticity and its regulatory pathways.more » « less
