The Landscape of Extreme Genomic Variation in the Highly Adaptable Atlantic Killifish

Abstract

Understanding and predicting the fate of populations in changing environments require knowledge about the mechanisms that support phenotypic plasticity and the adaptive value and evolutionary fate of genetic variation within populations. Atlantic killifish (Fundulus heteroclitus) exhibit extensive phenotypic plasticity that supports large population sizes in highly fluctuating estuarine environments. Populations have also evolved diverse local adaptations. To yield insights into the genomic variation that supports their adaptability, we sequenced a reference genome and 48 additional whole genomes from a wild population. Evolution of genes associated with cell cycle regulation and apoptosis is accelerated along the killifish lineage, which is likely tied to adaptations for life in highly variable estuarine environments. Genome-wide standing genetic variation, including nucleotide diversity and copy number variation, is extremely high. The highest diversity genes are those associated with immune function and olfaction, whereas genes under greatest evolutionary constraint are those associated with neurological, developmental, and cytoskeletal functions. Reduced genetic variation is detected for tight junction proteins, which in killifish regulate paracellular permeability that supports their extreme physiological flexibility. Low-diversity genes engage in more regulatory interactions than high-diversity genes, consistent with the influence of pleiotropic constraint on molecular evolution. High genetic variation is crucial for continued persistence of species given the pace of contemporary environmental change. Killifish populations harbor among the highest levels of nucleotide diversity yet reported for a vertebrate species, and thus may serve as a useful model system for studying evolutionary potential in variable and changing environments.

Profiling microRNA expression in Atlantic killifish (Fundulus heteroclitus) gill and responses to arsenic and hyperosmotic stress

“…iRNA were annotated using the miRMiner software (Tarver et al, 2013; Wheeler et al, 2009) and the killifish genome assembly (Reid et al, 2017). Using miRMiner, the clipped and length-filtered reads from all samples were collapsed into unique sequence tags.…”

“…Transcript 3’ UTR sequences were obtained for all annotated genes in the Fundulus heteroclitus genome (Reid et al, 2017) and the miRanda miRNA targeting algorithm was used to predict targets of miR-135b (Enright et al, 2003). A minimum score of 145 and maximum binding energy −15 kcal/mol were used as criteria for target identification.…”

“…Because they are non-migratory and have a small home range, distinct populations can be identified in relatively close geographic proximity to each other. This, in combination with their hardiness and amenability to laboratory conditions, has made killifish a particularly valuable vertebrate model for ecotoxicological studies (Bello et al, 2001; Di Giulio and Clark, 2015; Osterberg et al, 2018; Reid et al, 2017, 2016; Reitzel et al, 2014; Shaw et al, 2014; Whitehead et al, 2017). The genetic tools available for gene-environment interaction studies in killifish have recently expanded with the publication of a killifish reference genome (Burnett et al, 2007; Reid et al, 2017).…”

“…This, in combination with their hardiness and amenability to laboratory conditions, has made killifish a particularly valuable vertebrate model for ecotoxicological studies (Bello et al, 2001; Di Giulio and Clark, 2015; Osterberg et al, 2018; Reid et al, 2017, 2016; Reitzel et al, 2014; Shaw et al, 2014; Whitehead et al, 2017). The genetic tools available for gene-environment interaction studies in killifish have recently expanded with the publication of a killifish reference genome (Burnett et al, 2007; Reid et al, 2017). The sequenced genome enables investigation of gene regulatory mechanisms at multiple levels (genetic, epigenetic, transcriptional, post-transcriptional) that facilitate the ability of killifish to acclimate to changes in their environment, and in particular the role of non-coding RNAs, which have been identified as mediators of survival responses in organisms tolerant of environmental stress (Biggar and Storey, 2015).…”

Ryanodine receptor and FK506 binding protein 1 in the Atlantic killifish (Fundulus heteroclitus): A phylogenetic and population-based comparison

“…We utilized the recently released Fundulus genome (fundulus.org) (Reid et al, 2016; Reid et al, 2017) together with multiple large sequencing data sets to 1) characterize RyR and FKBP1 sequences present in the Fundulus genome, 2) determine the age and tissue specific mRNA expression of RyR and FKBP1 genes in killifish 3) evaluate the molecular phylogenetic relationships and key residue conservation, as it relates to PCB toxicity, between the RyR and FKBP1 in killifish and that of other model teleost and mammalian species and 4) determine whether killifish from NBH display genetic variation, including single nucleotide variants (SNV), in RyR and FKBP1 genes as compared to the SC reference population.…”