Biology subjects

Oleksiak, M. F.

Publications and source records attributed to Oleksiak, M. F..

5 recordsLinked to original sources

bioRxiv2023

Relentless Selection: The importance of within-generation selection in heterogeneous habitats

Natural selection relentlessly reshapes the genetic and phenotypic composition of populations, yet often adaptations cannot emerge due to excessive migration and gene flow. Nevertheless, in heterogeneous habitats strong selection could temporarily establish significant trait divergence among environmental patches. Here, we show that in Fundulus heteroclitus, a single generation of selection drives significant phenotypic divergence (5-15%) in organismal metabolic rate, cardiac metabolic rate and hypoxia tolerance. This divergence occurs among individuals of the same panmictic population residing in environmentally distinct microhabitats. Phenotypic divergence remains observable following long-term common-gardening and is supported by previous work documenting fine-scale, genetic divergence among microhabitat residents. We show that the magnitude of within-generation trait divergence is on the order of what is commonly observed among more isolated populations that have diverged over multiple generations. Although panmictic reproduction among microhabitat residents erodes trait divergence every generation, strong selection could potentially reestablish it in the next. In heterogeneous habitats, transient, fine-scale divergence could have a considerable impact on eco-evolutionary dynamics. Ignoring its contribution to overall trait variance could limit our ability to define meaningful, evolved divergence. SummaryNatural selection can lead to changes in organisms traits over time. Typically, these changes occur slowly over multiple generations and over large spatial scales. By studying a wild population of Atlantic killifish, we show that a single generation of natural selection can generate substantial trait variation over short distances. We observe significant differences in several physiological traits among individuals inhabiting distinct microhabitats in a patchy salt marsh environment. These differences are unlikely due to physiological acclimation and are best explained by strong, natural selection removing those individuals not suited to a particular microhabitat. Previous studies support natural selection as the most likely explanation, having shown subtle genetic differences among microhabitat residents. Remarkably, the magnitude of trait divergence is on the order of what is typically observed among populations that have diverged over multiple generations and larger spatial scales. Our results highlight the significant contribution of natural selection to trait variation in patchy environments, even over exceptionally short time and small spatial scales.

evolutionary biology↗

bioRxiv2022

mRNA expression explains metabolic and thermal physiology

Quantifying mRNA expression, which is heritable and physiologically inducible, reveals biologically important networks and pathways underlying complex traits. Here, we quantify mRNA expression in Fundulus heteroclitus, a small teleost fish, among three populations acclimated to 12{degrees}C and 28{degrees}C and relate it to variation in six, complex, physiological traits (whole animal metabolism (WAM), critical thermal maximum (CTmax), and four substrate specific cardiac metabolic rates (CaM)). Although 366 heart mRNAs and 528 brain mRNAs had significant differential expression between the two acclimation temperatures, none of the mRNA acclimation responses were shared across all three populations in any tissue. Yet, within an acclimation temperature across all three populations, weighted gene co-expression network analyses show that mRNA expression patterns explained WAM, CTmax, and CaM trait variation. These analyses revealed 9 significant heart MEs (first principal component of module expression) and 4 significant brain MEs. Heart MEs explained variation in WAM, CTmax, and two of the four substrate specific cardiac metabolic rates at 12{degrees}C, and CTmax at 28C. In contrast, brain MEs explained CTmax and WAM at 28{degrees}C but not at 12{degrees}C. Combining MEs as multiple correlations, 82% of variation in WAM at 12{degrees}C was explained by four heart MEs, 80% of variation in fatty-acid CaM at 12{degrees}C was explained by three heart MEs, and 72% of variation in CTmax at 28{degrees}C was explained by three brain MEs. These MEs were enriched for Kyoto Encyclopedia of Genes and Genomes (KEGG) terms related to specific metabolic pathways, suggesting that they represent biologically relevant pathways. Together these data suggest that mRNA co-expression explains complex traits; moreover, physiological traits are more reliant on heart expression at 12{degrees}C and brain expression at 28{degrees}C. Author SummaryDespite an abundance of genomic data, the molecular and genetic underpinnings of complex traits remain poorly understood. To better understand the molecular basis of complex traits, we used heart and brain mRNA expression to explain complex traits- physiological responses to temperature- in individuals collected from three saltmarsh fish (Fundulus heteroclitus) populations acclimated to 12{degrees}C and 28{degrees}C. We found that while physiological traits did not differ among populations, the mRNAs important for acclimation responses were >88% unique to a single population and differed between heart and brain tissues. We also found tissue specific co-expressed mRNAs that explain up to 82% of complex traits including whole animal metabolism, upper thermal tolerance, and substrate specific cardiac metabolism measured at 12{degrees}C or 28{degrees}C acclimation conditions. Notably, sets of co-expressed mRNAs related to these traits are enriched for molecular pathways affecting metabolism, giving insight into the molecular underpinnings of these traits.

genetics↗

bioRxiv2020

Rapid polygenic selection generates fine spatial structure among ecological niches in a well-mixed population

Evolution by natural selection may be effective enough to allow for recurrent, rapid adaptation to distinct niche environments within a well-mixed population. For this to occur, selection must act on standing genetic variation such that mortality i.e. genetic load, is minimized while polymorphism is maintained. Selection on multiple, redundant loci of small effect provides a potentially inexpensive solution. Yet, demonstrating adaptation via redundant, polygenic selection in the wild remains extremely challenging because low per-locus effect sizes and high genetic redundancy severely reduce statistical power. One approach to facilitate identification of loci underlying polygenic selection is to harness natural replicate populations experiencing similar selection pressures that harbor high within-, yet negligible among-population genetic variation. Such populations can be found among the teleost Fundulus heteroclitus. F. heteroclitus inhabits salt marsh estuaries that are characterized by high environmental heterogeneity e.g. tidal ponds, creeks, coastal basins. Here, we sample four of these heterogeneous niches (one coastal basin and three replicate tidal ponds) at two time points from among a single, panmictic F. heteroclitus population. We identify 10,861 single nucleotide polymorphisms using a genotyping-by-sequencing approach and quantify temporal allele frequency change within, as well as spatial divergence among subpopulations residing in these niches. We find a significantly elevated number of concordant allele frequency changes among all subpopulations, suggesting ecosystem-wide adaptation to a common selection pressure. Remarkably, we also find an unexpected number of temporal allele frequency changes that generate fine-scale divergence among subpopulations, suggestive of local adaptation to distinct niche environments. Both patterns are characterized by a lack of large-effect loci yet an elevated total number of significant loci. Adaptation via redundant, polygenic selection offers a likely explanation for these patterns as well as a potential mechanism for polymorphism maintenance in the F. heteroclitus system. Author SummaryEvolution by adaptation to local environmental conditions may occur more rapidly than previously thought. Recent studies show that natural selection is extremely effective when acting on, not one, but multiple genetic variants that are already present in a population. Here, we show that polygenic selection can lead to adaptation within a single generation by studying a wild, well-mixed population of mud minnows inhabiting environmentally distinct locations or niches (i.e. tidal ponds and coastal basins). We monitor allele proportions at over 10,000 genetic variants over time within a single generation and find a significant number to be changing substantially in every niche, suggestive of natural selection. We further demonstrate this genetic change to be non-random, generating mild, yet significant divergence between residents inhabiting distinct niches, indicative of local adaptation. We corroborate a previous study which discovered similar genetic divergence among niches during a different year, suggesting that local adaptation via natural selection occurs every generation. We show polygenic selection on standing genetic variation to be an effective and evolutionarily inexpensive mechanism, allowing organisms to rapidly adapt to their environments even at extremely short time scales. Our study provides valuable insights into the rate of evolution and the ability of organisms to respond to environmental change.

evolutionary biology↗

bioRxiv2020

Measuring complex phenotypes: A flexible high-throughput design for micro-respirometry

Variation in tissue-specific metabolism between species and among individuals is thought to be adaptively important; however, understanding this evolutionary relationship requires reliably measuring this trait in many individuals. In most higher organisms, tissue specificity is important because different organs (heart, brain, liver, muscle) have unique ecologically adaptive roles. Current technology and methodology for measuring tissue-specific metabolism is costly and limited by throughput capacity and efficiency. Presented here is the design for a flexible and cost-effective high-throughput micro-respirometer (HTMR) optimized to measure small biological samples. To verify precision and accuracy, substrate specific metabolism was measured in heart ventricles isolated from a small teleost, Fundulus heteroclitus, and in yeast (Saccharomyces cerevisiae). Within the system, results were reproducible between chambers and over time with both teleost hearts and yeast. Additionally, metabolic rates and allometric scaling relationships in Fundulus agree with previously published data measured with lower-throughput equipment. This design reduces cost, but still provides an accurate measure of metabolism in small biological samples. This will allow for high-throughput measurement of tissue metabolism that can enhance understanding of the adaptive importance of complex metabolic traits.

physiology↗

bioRxiv2020

An Innovative Setup for High-Throughput Respirometry of Small Aquatic Animals

AO_SCPLOWBSTRACTC_SCPLOWMetabolic rate is often measured as a phenotype in evolutionary genetics studies because it impacts organismal fitness, is repeatable and heritable, and is responsive to numerous environmental variables. Despite a wide body of literature about metabolic rates, key questions remain unanswered: 1) why do individuals from the same population exhibit up to three fold differences in metabolic rate, 2) how does metabolic rate change during an individuals lifetime, and 3) what metabolic rate is advantageous in a specific environment? Current low throughput approaches to measure metabolic rate make it difficult to answer these and other relevant ecological and evolutionary questions that require a much larger sample size. Here we describe a scalable high-throughput intermittent flow respirometer (HIFR) design and use it to measure the metabolic rates of 20 aquatic animals simultaneously while reducing equipment costs and time by more than 50%.

physiology↗