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Abstract Reconstructions of evolutionary history can be restricted by a lack of high-quality reference genomes. To date, only four of the eight species of bears (family Ursidae) have chromosome-level genome assemblies. Here, we present assemblies for three additional species—the sun, sloth, and Andean bears—and use a whole-genome alignment of all bear species and other carnivores to reconstruct the evolution of Ursidae. Multiple divergence dating approaches suggest that the six Ursine bears likely diversified in the last 5 Ma, but that divergence times within Ursinae are significantly impacted by gene tree heterogeneity. Consistent with this, we observe that nearly 50% of gene trees conflict with our highly supported species tree, a pattern driven by a significant early hybridization event within Ursinae. We also find that the karyotype of Ursinae is largely similar to the ancestral karyotype of all bears twenty million years prior. In contrast to this conservation of structure, dozens of chromosomal fissions and fusions associated with LINE/L1 retrotransposons dramatically restructured the genomes of the giant panda and Andean bear. Finally, we leverage these genomes to identify species-specific evidence for positive selection on genes associated with color, diet, and metabolism. One of these genes, TCPN2, has a role in pigmentation and shows a series of amino acid mutations in the polar bear over the last 0.5 Ma. Collectively, these new genomic resources enable improved reconstruction of the complex evolutionary history of bears and clarify how this enigmatic group diversified. 

Abstract Phased genomes and pangenomes are enhancing our understanding of genetic variation. Accurate phasing and assembly in repetitive regions of the genome remain challenging, however. Addressing this obstacle is crucial for studying structural genomic variation, such as copy number variations (CNVs) common to repetitive regions. Polar fishes, for example, evolved repetitive tandem arrays of antifreeze protein (AFP) genes that facilitate adaptation to freezing and expanded in copy number in colder environments. AFP CNVs remain poorly characterized in polar fishes and may be illuminated by haplotype-aware approaches. We performed long-read sequencing for two polar fishes in the suborder Zoarcoidei and leveraged additional published long-read data to assemble phased genomes. We developed a workflow to measure haplotype diversity in CNV while controlling for misassembly and switch errors—a change from one parental haplotype to another in a contiguous assembly. We presentgfa_parser, which computes and extracts all possible contiguous sequences for phased or primary assemblies from graphical fragment assembly (GFA) files, andswitch_error_screen, which flags potential switch errors.gfa_parserrevealed that assembly uncertainty was ubiquitous across AFP array haplotypes and that standard processing of graphical fragment assemblies can bias measurement of haplotype CNVs. We detected no switch errors in AFP arrays. After controlling for misassembly and switch error, we detected haplotype diversity of AFP CNVs in all studied polar Zoarcoidei species and in 60% of AFP arrays. Intraindividual haplotype diversity spanned differences of 3–16 copies. Our workflow revealed intraspecific genomic diversity in zoarcoids that likely fueled the evolution of AFP copy number across temperature. 

Abstract Antifreeze proteins (AFPs) have enabled teleost fishes to repeatedly colonize polar seas. Four AFP types have convergently evolved in several fish lineages. AFPs inhibit ice crystal growth and lower tissue freezing point. In lineages with AFPs, species inhabiting colder environments may possess more AFP copies. Elucidating how differences in AFP copy number evolve is challenging due to the genes’ tandem array structure and consequently poor resolution of these repetitive regions. Here, we explore the evolution of type III AFPs (AFP III) in the globally distributed suborder Zoarcoidei, leveraging six new long-read genome assemblies. Zoarcoidei has fewer genomic resources relative to other polar fish clades while it is one of the few groups of fishes adapted to both the Arctic and Southern Oceans. Combining these new assemblies with additional long-read genomes available for Zoarcoidei, we conducted a comprehensive phylogenetic test of AFP III evolution and modeled the effects of thermal habitat and depth on AFP III gene family evolution. We confirm a single origin of AFP III via neofunctionalization of the enzyme sialic acid synthase B. We also show that AFP copy number increased under low temperature but decreased with depth, potentially because pressure lowers freezing point. Associations between the environment and AFP III copy number were driven by duplications of paralogs that were translocated out of the ancestral locus at which AFP III arose. Our results reveal novel environmental effects on AFP evolution and demonstrate the value of high-quality genomic resources for studying how structural genomic variation shapes convergent adaptation. 

Abstract Parental exposure to environmental stress can influence phenotypic plasticity by offspring developing under that stressor. Transgenerational effects may also reshape natural selection on developmental plasticity by influencing its fitness consequences and expression of its genetic variation. We tested these hypotheses in the purple sea urchinStrongylocentrotus purpuratus, an invertebrate exposed to coastal upwelling (periods of low temperature and pH impacting biomineralization and performance). We conditioned parents and larvae to experimental upwelling and integrated RNA-seq, phenotyping of body size and biomineralization, and measured fitness-correlated traits in a quantitative genetic experiment. Larvae developing under upwelling induced widespread differential expression (DE), decreased biomineralization, and reduced body size. We detected fitness benefits for increased biomineralization and reduced size under upwelling indicative of adaptive plasticity, but only when larvae were spawned from parents exposed to upwelling. Larval DE was largely associated with adaptive phenotypic plasticity. Negative genetic correlation in DE was abundant between genes associated with adaptive plasticity. However, genetic correlations in DE associated with body size plasticity were significantly more positive in larvae from upwelling-exposed parents. These results show that transgenerational effects modify the fitness landscape and genetic architecture of phenotypic plasticity and its regulatory pathways. 

Abstract ObjectivesComplex physiological adaptations often involve the coordination of molecular responses across multiple tissues. Establishing transcriptomic resources for non-traditional model organisms with phenotypes of interest can provide a foundation for understanding the genomic basis of these phenotypes, and the degree to which these resemble, or contrast, those of traditional model organisms. Here, we present a one-of-a-kind gene expression dataset generated from multiple tissues of two hibernating brown bears (Ursus arctos). Data descriptionThis dataset is comprised of 26 samples collected from 13 tissues of two hibernating brown bears. These samples were collected opportunistically and are typically not possible to attain, resulting in a highly unique and valuable gene expression dataset. In combination with previously published datasets, this new transcriptomic resource will facilitate detailed investigation of hibernation physiology in bears, and the potential to translate aspects of this biology to treat human disease. 

Abstract There is great interest in exploring epigenetic modifications as drivers of adaptive organismal responses to environmental change. Extending this hypothesis to populations, epigenetically driven plasticity could influence phenotypic changes across environments. The canonical model posits that epigenetic modifications alter gene regulation and subsequently impact phenotypes. We first discuss origins of epigenetic variation in nature, which may arise from genetic variation, spontaneous epimutations, epigenetic drift, or variation in epigenetic capacitors. We then review and synthesize literature addressing three facets of the aforementioned model: (i) causal effects of epigenetic modifications on phenotypic plasticity at the organismal level, (ii) divergence of epigenetic patterns in natural populations distributed across environmental gradients, and (iii) the relationship between environmentally induced epigenetic changes and gene expression at the molecular level. We focus on DNA methylation, the most extensively studied epigenetic modification. We find support for environmentally associated epigenetic structure in populations and selection on stable epigenetic variants, and that inhibition of epigenetic enzymes frequently bears causal effects on plasticity. However, there are pervasive confounding issues in the literature. Effects of chromatin-modifying enzymes on phenotype may be independent of epigenetic marks, alternatively resulting from functions and protein interactions extrinsic of epigenetics. Associations between environmentally induced changes in DNA methylation and expression are strong in plants and mammals but notably absent in invertebrates and nonmammalian vertebrates. Given these challenges, we describe emerging approaches to better investigate how epigenetic modifications affect gene regulation, phenotypic plasticity, and divergence among populations. 

Abstract Under climate change, ectotherms will likely face pressure to adapt to novel thermal environments by increasing their upper thermal tolerance and its plasticity, a measure of thermal acclimation. Ectotherm populations with high thermal tolerance are often less thermally plastic, a trade‐off hypothesized to result from (i) a phenotypic limit on thermal tolerance above which plasticity cannot further increase the trait, (ii) negative genetic correlation or (iii) fitness trade‐offs between the two traits. Whether each hypothesis causes negative associations between thermal tolerance and plasticity has implications for the evolution of each trait.We empirically tested the limit and trade‐off hypotheses by leveraging the experimental tractability and thermal biology of the intertidal copepodTigriopus californicus. Using populations from four latitudinally distributed sites in coastal California, six lines per population were reared under a laboratory common garden for two generations. Ninety‐six full sibling replicates (n = 4–5 per line) from a third generation were developmentally conditioned to 21.5 and 16.5°C until adulthood. We then measured the upper thermal tolerance and fecundity of sibships at each temperature.We detected a significant trade‐off in fecundity, a fitness corollary, between baseline thermal tolerance and its plasticity.Tigriopus californicuspopulations and genotypes with higher thermal tolerance were less thermally plastic. We detected negative directional selection on thermal plasticity under ambient temperature evidenced by reduced fecundity. These fitness costs of plasticity were significantly higher among thermally tolerant genotypes, consistent with the trade‐off hypothesis. This trade‐off was evident under ambient conditions, but not high temperature.Observed thermal plasticity and fecundity were best explained by a model incorporating both the limit and trade‐off hypotheses rather than models with parameters associated with one hypothesis. Effects of population and family on tolerance and plasticity negatively covaried, suggesting that a negative genetic correlation could not be ruled as contributing to negative associations between the traits. Our study provides a novel empirical test of the fitness trade‐off hypothesis that leverages a strong inference approach. We discuss our results' insights into how thermal adaptation may be constrained by physiological limits, genetic correlations, and fitness trade‐offs between thermal tolerance and its plasticity. Read the freePlain Language Summaryfor this article on the Journal blog. 

Repetitive elements (REs) are integral to the composition, structure, and function of eukaryotic genomes, yet remain understudied in most taxonomic groups. We investigated REs across 601 insect species and report wide variation in RE dynamics across groups. Analysis of associations between REs and protein-coding genes revealed dynamic evolution at the interface between REs and coding regions across insects, including notably elevated RE–gene associations in lineages with abundant long interspersed nuclear elements (LINEs). We leveraged this large, empirical data set to quantify impacts of long-read technology on RE detection and investigate fundamental challenges to RE annotation in diverse groups. In long-read assemblies, we detected ∼36% more REs than short-read assemblies, with long terminal repeats (LTRs) showing 162% increased detection, whereas DNA transposons and LINEs showed less respective technology-related bias. In most insect lineages, 25%–85% of repetitive sequences were “unclassified” following automated annotation, compared with only ∼13% inDrosophilaspecies. Although the diversity of available insect genomes has rapidly expanded, we show the rate of community contributions to RE databases has not kept pace, preventing efficient annotation and high-resolution study of REs in most groups. We highlight the tremendous opportunity and need for the biodiversity genomics field to embrace REs and suggest collective steps for making progress toward this goal.