Marjorie F. Oleksiak

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 Summary: Evolution 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.

Metabolic 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 individual’s 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%.

In this paper, we used a Genotyping-by-Sequencing (GBS) approach to find and genotype more than 4000 genome-wide SNPs (Single Nucleotide Polymorphisms) from striped killifish exposed to a variety of polychlorinated biphenyls (PCBs) and other aromatic pollutants in New Bedford Harbor (NBH, Massachusetts, USA). The aims of this study were to identify the genetic consequences of exposure to aquatic pollutants and detect genes that may be under selection. Low genetic diversity (H_E and π) was found in the site exposed to the highest pollution level, but the pattern of genetic diversity did not match the pollution levels. Extensive connectivity was detected among sampling sites, which suggests that balanced gene flow may explain the lack of genetic variation in response to pollution levels. Tests for selection identified 539 candidate outliers, but many of the candidate outliers were not shared among tests. Differences among test results likely reflect different test assumptions and the complex pollutant mixture. Potentially, selectively important loci are associated with 151 SNPs, and enrichment analysis suggests a likely involvement of these genes with pollutants that occur in NBH. This result suggests that selective processes at genes targeted by pollutants may be occurring, even at a small geographical scale, and may allow the local striped killifish to resist the high pollution levels.

Examples of rapid evolution are common in nature but difficult to account for with the standard population genetic model of adaptation. Instead, selection from the standing genetic variation permits rapid adaptation via soft sweeps or polygenic adaptation. Empirical evidence of this process in nature is currently limited but accumulating. We provide genome-wide analyses of rapid evolution in Fundulus heteroclitus populations subjected to recently elevated temperatures due to coastal power station thermal effluents using 5449 SNPs across two effluent-affected and four reference populations. Bayesian and multivariate analyses of population genomic structure reveal a substantial portion of genetic variation that is most parsimoniously explained by selection at the site of thermal effluents. An FST outlier approach in conjunction with additional conservative requirements identify significant allele frequency differentiation that exceeds neutral expectations among exposed and closely related reference populations. Genomic variation patterns near these candidate loci reveal that individuals living near thermal effluents have rapidly evolved from the standing genetic variation through small allele frequency changes at many loci in a pattern consistent with polygenic selection on the standing genetic variation. While the ultimate trajectory of selection in these populations is unknown and we survey only a minority of genomic loci, our findings suggest that polygenic models of adaptation may play important roles in large, natural populations experiencing recent selection due to environmental changes that cause broad physiological impacts.

Marine genomics studies encompass diverse fields, which match the diversity of marine environments and the organisms that inhabit them. This diversity is not surprising because the world's oceans cover 70% of the world and contain approximately 2.2 million eukaryotic marine species [ 1 ]. This diversity means that there is no overarching theme that captures marine genomics. Yet, there are fundamental questions that are well-addressed using newly available genomic approaches with marine species. The five reviews in this issue explore genomic approaches, from evolutionary development in basal marine animals to population connectivity and adaptation to environmental change, and finally emphasize the need to go beyond genomics and tie in genomic data with integrative functional concepts.

We present a cost-effective approach to sequence whole mitochondrial genomes for hundreds of individuals. Our approach uses small reaction volumes and unmodified (non-phosphorylated) barcoded adaptors to minimize reagent costs. We demonstrate our approach by sequencing 383 Fundulus sp. mitochondrial genomes (192 F. heteroclitus and 191 F. majalis). Prior to sequencing, we amplified the mitochondrial genomes using 4–5 custom-made, overlapping primer pairs, and sequencing was performed on an Illumina HiSeq 2500 platform. After removing low quality and short sequences, 2.9 million and 2.8 million reads were generated for F. heteroclitus and F. majalis respectively. Individual genomes were assembled for each species by mapping barcoded reads to a reference genome. For F. majalis, the reference genome was built de novo. On average, individual consensus sequences had high coverage: 61-fold for F. heteroclitus and 57-fold for F. majalis. The approach discussed in this paper is optimized for sequencing mitochondrial genomes on an Illumina platform. However, with the proper modifications, this approach could be easily applied to other small genomes and sequencing platforms.

Acropora cervicornis, a threatened, keystone reef-building coral has undergone severe declines (>90 %) throughout the Caribbean. These declines could reduce genetic variation and thus hamper the species’ ability to adapt. Active restoration strategies are a common conservation approach to mitigate species' declines and require genetic data on surviving populations to efficiently respond to declines while maintaining the genetic diversity needed to adapt to changing conditions. To evaluate active restoration strategies for the staghorn coral, the genetic diversity of A. cervicornis within and among populations was assessed in 77 individuals collected from 68 locations along the Florida Reef Tract (FRT) and in the Dominican Republic. Genotyping by Sequencing (GBS) identified 4,764 single nucleotide polymorphisms (SNPs). Pairwise nucleotide differences (π) within a population are large (~37 %) and similar to π across all individuals. This high level of genetic diversity along the FRT is similar to the diversity within a small, isolated reef. Much of the genetic diversity (>90 %) exists within a population, yet GBS analysis shows significant variation along the FRT, including 300 SNPs with significant FST values and significant divergence relative to distance. There are also significant differences in SNP allele frequencies over small spatial scales, exemplified by the large FST values among corals collected within Miami-Dade county. Large standing diversity was found within each population even after recent declines in abundance, including significant, potentially adaptive divergence over short distances. The data here inform conservation and management actions by uncovering population structure and high levels of diversity maintained within coral collections among sites previously shown to have little genetic divergence. More broadly, this approach demonstrates the power of GBS to resolve differences among individuals and identify subtle genetic structure, informing conservation goals with evolutionary implications.

Background: The release of oil resulting from the blowout of the Deepwater Horizon (DH) drilling platform was one of the largest in history discharging more than 189 million gallons of oil and subject to widespread application of oil dispersants. This event impacted a wide range of ecological habitats with a complex mix of pollutants whose biological impact is still not yet fully understood. To better understand the effects on a vertebrate genome, we studied gene expression in the salt marsh minnow Fundulus grandis, which is local to the northern coast of the Gulf of Mexico and is a sister species of the ecotoxicological model Fundulus heteroclitus. To assess genomic changes, we quantified mRNA expression using high throughput sequencing technologies (RNA-Seq) in F. grandis populations in the marshes and estuaries impacted by DH oil release. This application of RNA-Seq to a non-model, wild, and ecologically significant organism is an important evaluation of the technology to quickly assess similar events in the future. Results: Our de novo assembly of RNA-Seq data produced a large set of sequences which included many duplicates and fragments. In many cases several of these could be associated with a common reference sequence using blast to query a reference database. This reduced the set of significant genes to 1,070 down-regulated and 1,251 up-regulated genes. These genes indicate a broad and complex genomic response to DH oil exposure including the expected AHR-mediated response and CYP genes. In addition a response to hypoxic conditions and an immune response are also indicated. Several genes in the choriogenin family were down-regulated in the exposed group; a response that is consistent with AH exposure. These analyses are in agreement with oligonucleotide-based microarray analyses, and describe only a subset of significant genes with aberrant regulation in the exposed set. Conclusion: RNA-Seq may be successfully applied to feral and extremely polymorphic organisms that do not have an underlying genome sequence assembly to address timely environmental problems. Additionally, the observed changes in a large set of transcript expression levels are indicative of a complex response to the varied petroleum components to which the fish were exposed.