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Abstract Evolutionary processes driving physiological trait variation depend on the underlying genomic mechanisms. Evolution of these mechanisms depends on the genetic complexity (involving many genes) and how gene expression impacting the traits is converted to phenotype. Yet, genomic mechanisms that impact physiological traits are diverse and context dependent (e.g., vary by environment and tissues), making them difficult to discern. We examine the relationships between genotype, mRNA expression, and physiological traits to discern the genetic complexity and whether the gene expression affecting the physiological traits is primarily cis- or trans-acting. We use low-coverage whole genome sequencing and heart- or brain-specific mRNA expression to identify polymorphisms directly associated with physiological traits and expressed quantitative trait loci (eQTL) indirectly associated with variation in six temperature specific physiological traits (standard metabolic rate, thermal tolerance, and four substrate specific cardiac metabolic rates). Focusing on a select set of mRNAs belonging to co-expression modules that explain up to 82% of temperature specific traits, we identified hundreds of significant eQTL for mRNA whose expression affects physiological traits. Surprisingly, most eQTL (97.4% for heart and 96.7% for brain) were trans-acting. This could be due to higher effect size of trans- versus cis-acting eQTL for mRNAs that are central to co-expression modules. That is, we may have enhanced the identification of trans-acting factors by looking for single nucleotide polymorphisms associated with mRNAs in co-expression modules that broadly influence gene expression patterns. Overall, these data indicate that the genomic mechanism driving physiological variation across environments is driven by trans-acting heart- or brain-specific mRNA expression. 

Abstract Physiological trait variation underlies health, responses to global climate change, and ecological performance. Yet, most physiological traits are complex, and we have little understanding of the genes and genomic architectures that define their variation. To provide insight into the genetic architecture of physiological processes, we related physiological traits to heart and brain mRNA expression using a weighted gene co-expression network analysis. mRNA expression was used to explain variation in six physiological traits (whole animal metabolism (WAM), critical thermal maximum (CT max ), and four substrate specific cardiac metabolic rates (CaM)) under 12 °C and 28 °C acclimation conditions. Notably, the physiological trait variations among the three geographically close (within 15 km) and genetically similar F. heteroclitus populations are similar to those found among 77 aquatic species spanning 15–20° of latitude (~ 2,000 km). These large physiological trait variations among genetically similar individuals provide a powerful approach to determine the relationship between mRNA expression and heritable fitness related traits unconfounded by interspecific differences. Expression patterns explained up to 82% of metabolic trait variation and were enriched for multiple signaling pathways known to impact metabolic and thermal tolerance ( e.g. , AMPK, PPAR, mTOR, FoxO, and MAPK) but also contained several unexpected pathways ( e.g. , apoptosis, cellular senescence), suggesting that physiological trait variation is affected by many diverse genes. 

ABSTRACT Physiology defines individual responses to global climate change and species distributions across environments. Physiological responses are driven by temperature on three time scales: acute, acclimatory and evolutionary. Acutely, passive temperature effects often dictate an expected 2-fold increase in metabolic processes for every 10°C change in temperature (Q10). Yet, these acute responses often are mitigated through acclimation within an individual or evolutionary adaptation within populations over time. Natural selection can influence both responses and often reduces interindividual variation towards an optimum. However, this interindividual physiological variation is not well characterized. Here, we quantified responses to a 16°C temperature difference in six physiological traits across nine thermally distinct Fundulus heteroclitus populations. These traits included whole-animal metabolism (WAM), critical thermal maximum (CTmax) and substrate-specific cardiac metabolism measured in approximately 350 individuals. These traits exhibited high variation among both individuals and populations. Thermal sensitivity (Q10) was determined, specifically as the acclimated Q10, in which individuals were both acclimated and assayed at each temperature. The interindividual variation in Q10 was unexpectedly large: ranging from 0.6 to 5.4 for WAM. Thus, with a 16°C difference, metabolic rates were unchanged in some individuals, while in others they were 15-fold higher. Furthermore, a significant portion of variation was related to habitat temperature. Warmer populations had a significantly lower Q10 for WAM and CTmax after acclimation. These data suggest that individual variation in thermal sensitivity reflects different physiological strategies to respond to temperature variation, providing many different adaptive responses to changing environments. 

Abstract Genetic data from nonmodel species can inform ecology and physiology, giving insight into a species’ distribution and abundance as well as their responses to changing environments, all of which are important for species conservation and management. Moreover, reduced sequencing costs and improved long-read sequencing technology allows researchers to readily generate genomic resources for nonmodel species. Here, we apply Oxford Nanopore long-read sequencing and low-coverage (∼1x) whole genome short-read sequencing technology (Illumina) to assemble a genome and examine population genetics of an abundant tropical and subtropical fish, the hardhead silverside (Atherinomorus stipes). These fish are found in shallow coastal waters and are frequently included in ecological models because they serve as abundant prey for commercially and ecologically important species. Despite their importance in sub-tropical and tropical ecosystems, little is known about their population connectivity and genetic diversity. Our A. stipes genome assembly is about 1.2 Gb with comparable repetitive element content (∼47%), number of protein duplication events, and DNA methylation patterns to other teleost fish species. Among five sampled populations spanning 43 km of South Florida and the Florida Keys, we find little population structure suggesting high population connectivity. 

To better understand temperature's role in the interaction between local evolutionary adaptation and physiological plasticity, we investigated acclimation effects on metabolic performance and thermal tolerance among natural Fundulus heteroclitus (small estuarine fish) populations from different thermal environments. Fundulus heteroclitus populations experience large daily and seasonal temperature variations, as well as local mean temperature differences across their large geographical cline. In this study, we use three populations: one locally heated (32°C) by thermal effluence (TE) from the Oyster Creek Nuclear Generating Station, NJ, and two nearby reference populations that do not experience local heating (28°C). After acclimation to 12 or 28°C, we quantified whole-animal metabolic (WAM) rate, critical thermal maximum (CT max ) and substrate-specific cardiac metabolic rate (CaM, substrates: glucose, fatty acids, lactate plus ketones plus ethanol, and endogenous (i.e. no added substrates)) in approximately 160 individuals from these three populations. Populations showed few significant differences due to large interindividual variation within populations. In general, for WAM and CT max , the interindividual variation in acclimation response (log 2 ratio 28/12°C) was a function of performance at 12°C and order of acclimation (12–28°C versus 28–12°C). CT max and WAM were greater at 28°C than 12°C, although WAM had a small change (2.32-fold) compared with the expectation for a 16°C increase in temperature (expect 3- to 4.4-fold). By contrast, for CaM, the rates when acclimatized and assayed at 12 or 28°C were nearly identical. The small differences in CaM between 12 and 28°C temperature were partially explained by cardiac remodeling where individuals acclimatized to 12°C had larger hearts than individuals acclimatized to 28°C. Correlation among physiological traits was dependent on acclimation temperature. For example, WAM was negatively correlated with CT max at 12°C but positively correlated at 28°C. Additionally, glucose substrate supported higher CaM than fatty acid, and fatty acid supported higher CaM than lactate, ketones and alcohol (LKA) or endogenous. However, these responses were highly variable with some individuals using much more FA than glucose. These findings suggest interindividual variation in physiological responses to temperature acclimation and indicate that additional research investigating interindividual may be relevant for global climate change responses in many species. 

Since 2014, corals within Florida’s Coral Reef have been dying at an unprecedented rate due to stony coral tissue loss disease (SCTLD). Here we describe the transcriptomic outcomes of three different SCTLD transmission experiments performed at the Smithsonian Marine Station and Mote Marine Laboratory between 2019 and 2020 on the corals Orbicella faveolata and Montastraea cavernosa. Overall, diseased O. faveolata had 2194 differentially expressed genes (DEGs) compared with healthy colonies, whereas diseased M. cavernosa had 582 DEGs compared with healthy colonies. Many significant DEGs were implicated in immunity, extracellular matrix rearrangement, and apoptosis. These included, but not limited to, peroxidases, collagens, Bax-like, fibrinogen-like, protein tyrosine kinase, and transforming growth factor beta. A gene module was identified that was significantly correlated to disease transmission. This module possessed many apoptosis and immune genes with high module membership indicating that a complex apoptosis and immune response is occurring in corals during SCTLD transmission. Overall, we found that O. faveolata and M. cavernosa exhibit an immune, apoptosis, and tissue rearrangement response to SCTLD. We propose that future studies should focus on examining early time points of infection, before the presence of lesions, to understand the activating mechanisms involved in SCTLD.