Fine-scale adaptive divergence and plasticity revealed by genetic and phenotypic variation in a marine invertebrate
ABSTRACT: The interplay between phenotypic plasticity and adaptive evolution has long been an important topic of evolutionary biology. This process is critical to our understanding of a species evolutionary potential in light of rapid climate changes. Despite recent theoretical work, empirical studies of natural populations, especially in marine invertebrates, are scarce. In this study, we investigated the relationship between adaptive divergence and plasticity by integrating genetic and phenotypic variation in Pacific oysters from its natural range in China. Genome resequencing of 371 oysters revealed unexpected fine-scale genetic structure that is largely consistent with phenotypic divergence in growth, physiology, thermal tolerance and gene expression across environmental gradient. These findings suggest that selection and local adaptation are pervasive and together with limited gene flow shape adaptive divergence. Plasticity in gene expression is positively correlated with evolved divergence, indicating that plasticity is adaptive and likely favored by selection in organisms facing dynamic environments such as oysters. Divergence in heat response and tolerance implies that the evolutionary potential to a warming climate differs among oyster populations. We suggest that trade-offs in energy allocation are important to adaptive divergence with acetylation playing a role in energy depression under thermal stress.
Project description:Temperature profoundly affects biological systems across all levels of organization. Over generations, species become evolutionarily adapted to specific thermal environments. In addition to evolved adaptive differences, individuals may reversibly modify their phenotype within their lifetimes in response to different thermal environments in a process termed phenotypic plasticity. The interaction between, evolutionary adaptation and phenotypic plasticity is complex and contentious. We utilize Fundulus glycolytic muscle physiology to address this interaction. We conducted a microarray analysis of muscle gene expression using three populations of Fundulus acclimated to three different temperatures. A phylogenetic comparative analysis among populations from different thermal environments demonstrates adaptive variation in mRNA expression for 186 genes. Sixty-seven genes had significant differences in mRNA expression in response to thermal acclimation. Interestingly, evolutionary adaptation and phenotypic plasticity appear to operate primarily orthogonally: few genes (although more than expected by chance alone) exhibit both adaptive variation and phenotypic plasticity. The magnitude and function of the adaptive variation in gene expression is dependent on acclimation temperature (e.g., more genes have adaptive differences at 12° and 28°C than at 20°C), demonstrating the importance of gene-by-environment interactions. Finally, a functional analysis of gene expression provides novel, testable hypotheses regarding adaptation of muscle physiology. Overall design: A loop design was used for the microarray hybridizations. The loop consisted of 56 individual labeled with Cy3 and Cy5 aRNAs for three populations acclimated to three temperatures (12°C, 20°C 28°C). The loop formed was MA→GA→Fg→ME..., where each arrow represents a separate hybridization (array) with the biological sample at the base of the arrow labeled with Cy3 and the biological sample at the head of the arrow labeled with Cy5. ME are F. heteroclitus individuals from Maine, GA are F. heteroclitus individuals from Georgia, and Fg are F. grandis individuals from Florida. Acclimation temperatures and individuals randomized within this loop. Slides were scanned using a ScanArray Express with 5um resolution at half speed. Images were quantitated using ImaGene software.
Project description:The goals of these studies are to explore the mechanisms that enable extreme physiological plasticity and that may account for evolutionary divergence of adaptive osmotic physiologies among taxa that occupy different osmotic niches. In a common-garden environment, we track physiological and genome expression responses to hypo-osmotic (freshwater) challenge during a time-course of acclimation, and contrast these responses within and between species. We seek to identify mechanisms that facilitate osmotic acclimation that are evolutionarily conserved between basal and derived physiologies, and identify mechanisms that are uniquely derived to enable the extreme osmotic plasticity exhibited by F. heteroclitus. Importantly, previous studies using a comparable experimental design have identified physiological changes and genome expression responses that are adaptive for populations of F. heteroclitus that live in fresh water. As such, this enables us to test whether mechanisms of adaptive micro-evolutionary divergence across osmotic gradients within F. heteroclitus are shared with the mechanisms that account for patterns of macro-evolutionary divergence between F. heteroclitus and F. majalis that we identify in this study. That is, are the targets of micro-evolutionary fine-tuning the same or different as the targets of macro-evolutionary divergence across osmotic boundaries? Population comparisons include between populations from Chesapeake Bay (CB), coastal Virginia (VA), and coastal Georgia (GA).
Project description:We used microarrays to investigate the transcriptome of 6 days old male flies exposed to either 15 or 25 C development at either constant or fluctuating temperatures. Further, we investigated gene expression at benign (20C) and high (35C) temperatures With global climate change temperature means and variability are expected to increase. Thus, exposures to elevated temperatures are expected to become an increasing challenge for terrestrial ectotherm populations. While evolutionary adaptation seems to be constrained or proceed at an insufficient pace, many populations are expected to rely on phenotypic plasticity (thermal acclimation) for coping with the predicted changes. However, the effects of fluctuating temperature on the molecular mechanisms and the implications for heat tolerance are not well understood. To understand and predict consequences of climate change it is important to investigate how different components of the thermal environment, including fluctuating thermal conditions, contribute to changes in thermal acclimation. In this study we investigated the impact of mean and diurnal fluctuation of temperature on heat tolerance in Drosophila melanogaster and on the underlying molecular mechanisms in adult male flies. Flies from two constant and two ecologically relevant fluctuating temperature regimes were tested for their critical thermal maxima (CTmax) and associated global gene expression profiles at benign and thermally stressful conditions. Both temperature parameters contributed independently to the thermal acclimation, with regard to heat tolerance as well as the global gene expression profile. Although the independent transcriptional effects caused by fluctuations were relatively small, they are likely to be essential for our understanding of thermal adaptation. Thus, high temperature acclimation ability might not be measured correctly and might even be underestimated at constant temperatures. Our data suggests that the particular mechanisms affected by thermal fluctuations are related to phototransduction and environmental sensing. Thus genes and pathways involved in those processes are likely to be of major importance in a future warmer and more fluctuating climate. Eight experimental groups were analyzed in triplicate, in total 24 Affymetrix GeneChip Drosophila Genome 2.0 Arrays
Project description:As a result of increasing thermal fluctuations and mean temperature values, organisms will experience conditions beyond their physiological limits. In situ adaptation to thermal regimes is mediated via directional selection and phenotypic plasticity. The latter involves physiological and morphological adjustments realized by underlying molecular mechanisms. Understanding species' adaptive capacities requires investigating these adjustive processes. Yet, acclimation through phenotypic plasticity remains largely unexplored, especially at the molecular level; For example, whether cold-adapted species inhabiting freshwater spring ecosystems have evolved adaptive mechanisms to cope with warming of freshwater habitats has, to our knowledge, never been investigated. This work reports a comprehensive proteomics study of the stenotopic species Crunoecia irrorata (Curtis, 1834) (Trichoptera: Lepistomatidae) acclimated to 10, 15 and 20 °C for 168 h. A liquid chromatography tandem mass spectrometry (LC-MS/MS)-based shotgun proteomics approach identified molecular mechanisms underlying acclimation. We constructed a homology-based database by combining genomic and transcriptomic data from related species and quantified 1356 proteins, of which 186 were differentially expressed between temperature treatments. Through functional annotation, we identified candidate proteins facilitating, among others, trehalose accumulation, tracheal system alteration, and heat shock protein regulation, then discuss concomitant ecophysiological implications. These results provide new insights into the mechanisms of adaptive responses to warming of species inhabiting freshwater ecosystems sensitive to climate change. Further, identified candidate proteins will aid in developing targeted experiments to understand their compensatory physiology. To our knowledge, this is the first study utilizing this approach to investigate the nature of phenotypic plasticity of aquatic macroinvertebrates.
Project description:We examined adaptive morphological divergence and epigenetic variation in genetically impoverished asexual populations of a freshwater snail, Potamopyrgus antipodarum from distinct environments. These populations exhibit environment-specific adaptive divergence in shell shape and significant genome wide DNA methylation differences among differentially adapted lake and fast water flow river populations. The epigenetic variation correlated with adaptive phenotypic variation in rapidly adapting asexual animal populations. This provides one of the first examples of environmentally-driven differences in epigenetics that associates with adaptive phenotypic divergence. Overall design: To examine the association between this adaptive divergence and epigenetic differences, we sampled at least 30 individuals from a “river” site characterized by constantly fast water current speeds due to input from underground springs (Ritter Island, Snake River, ID) and from a “lake” site with no water current (Lake Lytle, Rockaway Beach, OR). Shell spire height and aperture length were measured as an index of adaptive foot size and shell shape differences. On these same samples, we dissected foot tissue from individuals for the analysis of epigenetic variation.
Project description:We examined adaptive morphological divergence and epigenetic variation in genetically impoverished asexual populations of a freshwater snail, Potamopyrgus antipodarum from distinct environments. These populations exhibit environment-specific adaptive divergence in shell shape and significant genome wide DNA methylation differences among differentially adapted lake and fast water flow river populations. The epigenetic variation correlated with adaptive phenotypic variation in rapidly adapting asexual animal populations. This provides one of the first examples of environmentally-driven differences in epigenetics that associates with adaptive phenotypic divergence. Overall design: To examine the association between this adaptive divergence and epigenetic differences, we sampled at least 30 individuals from a “river” site characterized by constantly fast water current speeds due to input from underground springs (Ritter Island, Snake River, ID) and from a “lake” site with no water current (Lake Washington, Seattle, WA). Shell spire height and aperture length were measured as an index of adaptive foot size and shell shape differences. On these same samples, we dissected foot tissue from individuals for the analysis of epigenetic variation.
Project description:Although the relationship between phenotypic plasticity and evolutionary dynamics has attracted large interest, very little is known about the contribution of phenotypic plasticity to adaptive evolution. In this study, we analyzed phenotypic and genotypic changes in E. coli cells during adaptive evolution to ethanol stress. To quantify the phenotypic changes, transcriptome analyses were performed. We previously obtained 6 independently evolved ethanol tolerant E. coli strains, strains A through F, by culturing cells under 5% ethanol stress for about 1000 generations and found a significantly larger growth rate than the parent strains (Horinouchi et al, 2010, PMID: 20955615). To elucidate the phenotypic changes that occurred during adaptive evolution, we quantified the time-series of the expression changes by microarray analysis. Starting from frozen stocks obtained at 6 time points (0, 384, 744, 1224, 1824 and 2496 hours) in laboratory evolution, cells were cultured under 5% ethanol stress, and mRNA samples were obtained in the exponential growth phase for microarray analysis.
Project description:Traditionally, the study of evolution has focused on heritable variation, because selection on non-heritable phenotypic variation was deemed non-important for its inability to cause evolutionary responses such as diversification of lineages. Recently however, it has been suggested that also environmentally induced phenotypic variation such as phenotypic plasticity can play an important role in adaptive responses resulting in diversification. The purpose of this study is to investigate the importance of phenotypic plasticity for the diversification of lineages, using life history, morphological traits, and genomic profiling during post embryonic development in plastic and non-plastic genotypes of the common frog Rana temporaria. Six animals each originating from four different islands were reared in either constant or reduced water conditions and hepatic mRNA levels of Gosner stage 37 animals evaluated by MAGEX DNA array analysis.
Project description:Despite the progress achieved in elucidating the ecological mechanisms of adaptive radiation, there has been little focus on documenting the extent of adaptive differentiation in physiological functions during this process. Moreover, a thorough understanding of the genomic basis underlying phenotypic adaptive divergence is still in its infancy. One important evolutionary process for which causal genetic mechanisms are largely unknown pertains to life-history trade-offs. We analysed patterns of gene transcription in liver tissue of sympatric dwarf and normal whitefish from two natural lakes, as well as from populations reared in controlled environments, using a 16 006-gene cDNA microarray in order to: (i) document the extent of physiological adaptive divergence between sympatric dwarf and normal species pairs, and (ii) explore the molecular mechanisms of differential life history trade-offs between growth and survival potentially involved in their adaptive divergence. In the two natural lakes, 6.45% of significantly transcribed genes showed regulation either in parallel fashion (2.39%) or in different directions (4.06%). Among genes showing parallelism in regulation patterns, we observed a higher proportion of over-expressed genes in dwarf relative to normal whitefish (70.6%). Patterns observed in controlled conditions were also generally congruent with those observed in natural populations. Dwarf whitefish consistently showed significant over-expression of genes potentially associated with survival through enhanced activity (energy metabolism, iron homeostasis, lipid metabolism, detoxification), whereas more genes associated with growth (protein synthesis, cell cycle, cell growth) were generally down-regulated in dwarf relative to normal whitefish. Overall, parallelism in patterns of gene transcription, as well as patterns of interindividual variation across controlled and natural environments, provide strong indirect evidence for the role of selection in the evolution of differential regulation of genes involving a vast array of potentially adaptive physiological processes between dwarf and normal whitefish. Our results also provide a first mechanistic, genomic basis for the observed trade-off in life-history traits distinguishing dwarf and normal whitefish species pairs, wherein enhanced survival via more active swimming, necessary for increased foraging and predator avoidance, engages energetic costs that translate into slower growth rate and reduced fecundity in dwarf relative to normal whitefish. Overall design: Direct comparison of Dwarf vs Normal ecotypes. Samples comes from two natural environments (two different lakes) and one controled environement.
Project description:Global climate change increasingly polarizes environments, presenting unprecedented challenges to many organisms (Smol, 2012). Polarization occurs not only in the spatial dimension, producing greater desert drought and tropical rainfall, for example, but also in the temporal dimension by making a local environment more variable over time. Many organisms survive these fluctuating environmental conditions by manifesting multiple distinct phenotypes through developmental processes that enable phenotypic plasticity (Pigliucci et al., 2006; Parsons et al., 2011). As with early development, these processes are expected to strictly regulate gene expression to canalize phenotype, despite the genetic diversity within populations (Alberch, 1982; Riska, 1986, Pigliucci et al., 1996). For plasticity to evolve, natural selection must act on genes that regulate trait variation, e.g, those conferring norms of reaction to a specific set of conditions. Despite the importance of these reaction norms for coping with environmental challenges, the genetic framework underlying phenotypic plasticity remains poorly defined, making it impossible to study how they function, differ among natural populations, and evolve. Here we used arsenic, a chemical inhibitor of salinity acclimation, to identify genes involved in transforming the gill from its freshwater to its seawater architecture in the euryhaline teleost Fundulus heteroclitus. Linear model interaction terms associated with the combined effect of arsenic and salinity challenge revealed an antagonistic relationship between arsenic exposure and salinity acclimation Exposure to arsenic during salinity acclimation yielded gene expression values similar to those observed in unexposed fish that remained in a stable environment, demonstrating that arsenic prevents changes in gene expression that normally enable osmotic plasticity. The gene sets defined by the interaction terms showed reduced inter-individual variation, suggesting unusually tight control, consistent with the hypothesis that they participate in a canalized developmental response. Evidence that natural selection acts to preserve their canalized gene expression was obtained by referencing three populations that differ in their adaptive tolerance to salinity changes (Whitehead et al., 2011). Specifically, populations adapted to withstand the widest salinity range showed both reduced transcriptional variation in genes enabling gill plasticity and an increased osmoregulatory capacity, highlighted by more stable plasma chloride concentrations in response to an osmotic challenge. Finally, we observed significantly fewer associations between genes underlying trait variation and their transcriptional regulators compared to genes that responded to only arsenic or salinity. Collectively, our results demonstrate that phenotypic plasticity converges on a molecular solution that parallels early development, in which the expression of phenotypic plasticity genes and phenotypes are canalized in part by reducing trans-regulatory complexity. 36 Sample comparisons with fish gills exposed to freshwater, freshwater to seawater for 1 hour, freshwater to seawater for 1 hour with arsenic, freshwater to seawater for 24 hours, freshwater to seawater for 24 hours with arsenic, and freshwater with arsenic for 48 hours