Physiological plasticity and adaptive evolution may facilitate persistence in a changing environment. As a result, there is an interest in understanding species' capacities for plastic and evolved responses, and the mechanisms by which these responses occur. Transcriptome sequencing has become a powerful tool for addressing these questions, providing insight into otherwise unobserved effects of changing conditions on organismal physiology and variation in these effects among individuals and populations. Here, we review recent studies using comparative transcriptomics to understand plastic and evolutionary responses to changing environments. We focus on 2 areas where transcriptomics has played an important role: first, in understanding the genetic basis for local adaptation to current gradients as a proxy for future adaptation, and second, in understanding organismal responses to multiple stressors. We find most studies examining multiple stressors have tested the effects of each stressor individually; the few studies testing multiple stressors simultaneously have found synergistic effects on gene expression that would not have been predicted from single stressor studies. We discuss the importance of robust experimental design to allow for a more sophisticated characterization of transcriptomic responses and conclude by offering recommendations for future research, including integrating genomics with transcriptomics, testing gene regulatory networks, and comparing the equivalence of transcription to translation and the effects of environmental stress on the proteome.
ANISEED (https://www.aniseed.cnrs.fr) is the main model organism database for the worldwide community of scientists working on tunicates, the vertebrate sister-group. Information provided for each species includes functionally-annotated gene and transcript models with orthology relationships within tunicates, and with echinoderms, cephalochordates and vertebrates. Beyond genes the system describes other genetic elements, including repeated elements and cis-regulatory modules. Gene expression profiles for several thousand genes are formalized in both wild-type and experimentally-manipulated conditions, using formal anatomical ontologies. These data can be explored through three complementary types of browsers, each offering a different view-point. A developmental browser summarizes the information in a gene- or territory-centric manner. Advanced genomic browsers integrate the genetic features surrounding genes or gene sets within a species. A Genomicus synteny browser explores the conservation of local gene order across deuterostome. This new release covers an extended taxonomic range of 14 species, including for the first time a non-ascidian species, the appendicularian Oikopleura dioica. Functional annotations, provided for each species, were enhanced through a combination of manual curation of gene models and the development of an improved orthology detection pipeline. Finally, gene expression profiles and anatomical territories can be explored in 4D online through the newly developed Morphonet morphogenetic browser.
Summary Organisms may respond to changing environments through phenotypic plasticity or adaptive evolution. These two processes are not mutually exclusive and may either dampen or strengthen each other's effects, depending on the genetic correlation between trait values and the slopes of their norms of reaction. To examine the effect of adaptation to heat stress on the plasticity of heat tolerance, we hybridized populations of the crustacean Tigriopus californicus that show divergent phenotypes for heat tolerance. We then selected for increased heat tolerance in hybrids and measured heat tolerance and the phenotypic plasticity of heat tolerance in both selected lines and unselected controls. To test whether the changes in phenotypic plasticity were associated with changes in the plasticity of gene expression, we also sequenced transcriptomes of selected and unselected lines, both under heat shock and at ambient temperatures. We observed increased heat tolerance in selected lines, but also lower phenotypic and transcriptional plasticity in response to heat stress. The plastic response to heat stress was highly enriched for hydrolytic and catalytic activities, suggesting a prominent role for degradation of misfolded proteins. Our findings have important implications for biological responses to climate change: if adaptation to environmental stress reduces plasticity, then plasticity and adaptive evolution will make overlapping, rather than additive contributions to buffering populations from environmental change.
Trade‐offs may influence both physiological and evolutionary responses to co‐occurring stressors, but their effects on both plastic and adaptive responses to climate change are poorly understood. To test for genetic and physiological trade‐offs incurred in tolerating multiple stressors, we hybridized two populations of the intertidal copepod Tigriopus californicus that were divergent for both heat and salinity tolerance. Starting in the F2 generation, we selected for increased tolerance of heat, low salinity, and high salinity in replicate lines. After five generations of selection, heat‐selected lines had greater heat tolerance but lower fecundity, indicating an energetic cost to tolerance. Lines selected for increased salinity tolerance did not show evidence of adaptation to their respective environments; however, hypo‐osmotic selection lines showed substantial loss of tolerance to hyperosmotic stress. Neither of the salinity selection regimes resulted in diminished heat tolerance at ambient salinity; however, simultaneous exposure to heat and hypo‐osmotic stress led to decreased heat tolerance, implying a physiological trade‐off in tolerance to the two stressors. When we quantified the transcriptomic response to heat and salinity stress via RNA sequencing, we observed little overlap in the stress responses, suggesting the observed synergistic effects of heat and salinity stress were driven by competing energetic demands, rather than shared stress response pathways.
The origin of novel traits can promote expansion into new niches and drive speciation. Ctenophores (comb jellies) are unified by their possession of a novel cell type: the colloblast, an adhesive cell found only in the tentacles. Although colloblast-laden tentacles are fundamental for prey capture among ctenophores, some species have tentacles lacking colloblasts and others have lost their tentacles completely. We used transcriptomes from 36 ctenophore species to identify gene losses that occurred specifically in lineages lacking colloblasts and tentacles. We cross-referenced these colloblast- and tentacle-specific candidate genes with temporal RNA-Seq during embryogenesis in Mnemiopsis leidyi and found that both sets of candidates are preferentially expressed during tentacle morphogenesis. We also demonstrate significant upregulation of candidates from both data sets in the tentacle bulb of adults. Both sets of candidates were enriched for an N-terminal signal peptide and protein domains associated with secretion; among tentacle candidates we also identified orthologs of cnidarian toxin proteins, presenting tantalizing evidence that ctenophore tentacles may secrete toxins along with their adhesive. Finally, using cell lineage tracing, we demonstrate that colloblasts and neurons share a common progenitor, suggesting the evolution of colloblasts involved co-option of a neurosecretory gene regulatory network. Together these data offer an initial glimpse into the genetic architecture underlying ctenophore cell-type diversity.
Conflicting patterns of population differentiation between the mitochondrial and nuclear genomes (mito-nuclear discordance) have become increasingly evident as multilocus data sets have become easier to generate. Incomplete lineage sorting (ILS) of nucDNA is often implicated as the cause of such discordance, stemming from the large effective population size of nucDNA relative to mtDNA. However, selection, sex-biased dispersal and historical demography can also lead to mito-nuclear discordance. Here, we compare patterns of genetic diversity and subdivision for six nuclear protein-coding gene regions to those for mtDNA in a common Caribbean coral reef sponge, Callyspongia vaginalis, along the Florida reef tract. We also evaluated a suite of summary statistics to determine which are effective metrics for comparing empirical and simulated data when testing drivers of mito-nuclear discordance in a statistical framework. While earlier work revealed three divergent and geographically subdivided mtDNACOI haplotypes separated by 2.4% sequence divergence, nuclear alleles were admixed with respect to mitochondrial clade and geography. Bayesian analysis showed that substitution rates for the nuclear loci were up to 7 times faster than for mitochondrial COI. Coalescent simulations and neutrality tests suggested that mito-nuclear discordance in C. vaginalis is not the result of ILS in the nucDNA or selection on the mtDNA but is more likely caused by changes in population size. Sperm-mediated gene flow may also influence patterns of population subdivision in the nucDNA.
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