Anna Tigano

Despite widespread declines of many wildlife species, the effects of population decline on the genome and the recovery potential of affected species are still poorly understood, especially beyond a few charismatic species. The Northern abalone (or Pinto abalone; Haliotis kamtschatkana ) is a marine gastropod mollusk of social, cultural and historical economic importance in the Pacific Northwest of North America that experienced a decline in population density due to commercial harvest, and is currently listed as endangered in Canada under the Species at Risk Act. Previous genetic investigations based on microsatellites and reduced‐representation approaches concluded that Northern abalone is panmictic throughout its range, from Alaska to California, and identified high levels of genetic variation with no indication of population decline. Using whole genome resequencing data from Northern abalone sampled across the northern part of the species range, we instead identified both: (1) significant differentiation between two genetic groups, albeit concentrated in few genomic regions, and (2) a strong signature of a dramatic population decline, without genomic evidence of genetic inbreeding. Demographic reconstructions showed a modest signal of recent population expansion, supported by an increasing number of juveniles observed during dive surveys. We also found evidence of historical, rather than current, connectivity throughout the area investigated. These results are important for management decisions and highlight the utility of whole genome data in conservation, especially in species with historically large effective population sizes like the Northern abalone.

Whole‐genome sequencing (WGS) has greatly expanded researchers' ability to study structural variants (SVs), that is, the variation in the presence, number, orientation or position of a DNA sequence. This has paved the way to study the eco‐evolutionary dynamics of SVs across the tree of life and within a population genomics framework. In this review, we provide the necessary fundamentals to help researchers generate and analyse population‐level SV data. We discuss the unique properties of different SV groups and how these fundamental differences interact with important biological and evolutionary processes using both empirical results and theory. This includes discussion of unresolved issues around SVs, such as technical difficulties in identification, accounting for diversity and evaluating functional effects. We explicitly integrate into this discussion transposable elements, which are an important component of SVs often identified in population‐level variant data. Finally, we focus on the practical side of SV analysis, offering a framework for SV identification and data analysis. In particular, we examine the heterogeneous nature of SV properties (type, length, sequence identity) that should be considered when studying them in ecology and evolution. This review aims to provide resources and guidelines to help researchers navigate the complexities of a relatively new field of eco‐evolutionary genomics research.

Despite widespread declines of many wildlife species, the effects of population decline on the genetic health and the recovery potential of affected species is still poorly understood, especially beyond a few charismatic species. The Northern abalone (or Pinto abalone; Haliotis kamtschatkana) is a marine gastropod mollusc of social, cultural and historical economic importance in the Pacific Northwest of North America that experienced a decline in population density due to commercial harvest and is currently listed as endangered in Canada under the Species at Risk Act. Previous genetic investigations based on microsatellites and reduced-representation approaches concluded that Northern abalone is panmictic throughout its range, from Alaska to California, and identified high levels of genetic variation with no indication of population decline. Using whole genome resequencing data from Northern abalone sampled across the northern part of the species range, we instead identified both: 1) significant differentiation between two genetic groups, albeit very concentrated in the genome; and 2) a strong signature of a dramatic population decline, without evidence of genetic inbreeding. Even though demographic reconstructions showed a timid signal of recent population expansion, the pervasive excess of rare alleles identified (including a high occurrence of singletons) may pose a genetic load risk, potentially hindering the species recovery. We also found evidence of historical, rather than current, connectivity throughout the area investigated. These results are important for management decisions and highlight the utility of whole genome data in conservation, especially in species with historically large effective population sizes like the Northern abalone.

The impact of genome structure on adaptation is a growing focus in evolutionary biology, revealing an important role for structural variation and recombination landscapes in shaping genetic diversity across genomes and among populations. This is particularly relevant when local adaptation occurs despite gene flow, where clustering of differentiated loci can maintain locally adapted variants by reducing recombination between them. However, the limited genomic resources for nonmodel species, including reference genomes and recombination maps, have constrained our understanding of these patterns. In this study, we leverage the Atlantic silverside—a nonmodel fish with extensive local adaptation across a steep latitudinal gradient—as an ideal system to explore how genome structure influences adaptation under varying levels of gene flow, using a newly available reference genome and multiple recombination maps. Analyzing 168 genomes from four populations, we found a continuum of genome-wide differentiation increasing from south to north, reflecting higher connectivity among southern populations and reduced gene flow at northern latitudes. With increasing gene flow, the number and clustering of FST outlier loci also increased, with differentiated loci found exclusively within large haploblocks harboring inversions and smaller peaks overlapping putative centromeric regions. Notably, sequence divergence was only evident in inversions, supporting their role in adaptive divergence with gene flow, whereas centromeric regions appeared differentiated because of low recombination and diversity, with no indication of elevated divergence. Our results support the hypothesis that clustered genomic architectures evolve with high gene flow and enhance our understanding of how inversions and centromeres are linked to different evolutionary processes.

The impact of genome structure on adaptation is a growing focus in evolutionary biology, revealing an important role for structural variation and recombination landscapes in shaping genetic diversity across genomes and among populations. This is particularly relevant when local adaptation occurs despite gene flow, where clustering of differentiated loci can maintain locally adapted variants by reducing recombination between them. However, the limited genomic resources for non-model species, including reference genomes and recombination maps, has constrained our understanding of these patterns. In this study, we leverage the Atlantic silverside—a non-model fish with extensive local adaptation across a steep latitudinal gradient—as an ideal system to explore how genome structure influences adaptation under varying levels of gene flow, using a newly available reference genome and multiple recombination maps. Analyzing 168 genomes from four populations, we found a continuum of genome-wide differentiation increasing from south to north, reflecting higher connectivity among southern populations and reduced gene flow at northern latitudes. With increasing gene flow, the number and clustering of F _ST outlier loci also increased, with differentiated loci tightly clustered in large haploblocks harboring inversions and smaller peaks overlapping putative centromeres. Notably, sequence divergence was only evident in inversions, supporting their role in adaptive divergence with gene flow, whereas centromeres appeared differentiated because of low recombination and reduced diversity, with no indication of elevated sequence divergence. Our results support the hypothesis that clustered genomic architectures evolve with high gene flow and enhance our understanding of how inversions and centromeres are linked to different evolutionary processes. Significance Statement: How populations preserve favorable combinations of genes adapted to their local environment despite reproducing with populations adapted to different conditions is a longstanding question in evolutionary biology. By analyzing the genomes of 168 Atlantic silverside fish from four populations, we found that when populations adapted to different environments frequently interbreed, genetic differences concentrate in specific parts of the genome, particularly in chromosomal inversions—where segments of DNA are flipped. These inversions help preserve locally adapted gene combinations, enabling populations to maintain differences essential for survival in their habitats. This research enhances our understanding of genomic adaptation, a fundamental evolutionary question with increasing relevance as environmental changes pose new challenges globally.

Understanding the adaptive potential of populations and species is pivotal for minimizing the loss of biodiversity in this era of rapid climate change. Adaptive potential has been estimated in various ways, including based on levels of standing genetic variation, presence of potentially beneficial alleles, and/or the severity of environmental change. Kokanee salmon, the non‐migratory ecotype of sockeye salmon (Oncorhynchus nerka), is culturally and economically important and has already been impacted by the effects of climate change. To assess its climate vulnerability moving forward, we integrated analyses of standing genetic variation, genotype‐environment associations, and climate modeling based on sequence and structural genomic variation from 224 whole genomes sampled from 22 lakes in British Columbia and Yukon (Canada). We found that variables for extreme temperatures, particularly warmer temperatures, had the most pervasive signature of selection in the genome and were the strongest predictors of levels of standing variation and of putatively adaptive genomic variation, both sequence and structural. Genomic offset estimates, a measure of climate vulnerability, were significantly correlated with higher increases in extreme warm temperatures, further highlighting the risk of summer heat waves that are predicted to increase in frequency in the future. Levels of standing genetic variation, an important metric for population viability and resilience, were not correlated with genomic offset. Nonetheless, our combined approach highlights the importance of integrating different sources of information and genomic data to formulate more comprehensive and accurate predictions on the vulnerability of populations and species to future climate change.

Amidst the current biodiversity crisis, the availability of genomic resources for declining species can provide important insights into the factors driving population decline. In the early 1990s, the black-legged kittiwake (Rissa tridactyla), a pelagic gull widely distributed across the arctic, subarctic, and temperate zones, suffered a steep population decline following an abrupt warming of sea surface temperature across its distribution range and is currently listed as Vulnerable by the International Union for the Conservation of Nature. Kittiwakes have long been the focus for field studies of physiology, ecology, and ecotoxicology and are primary indicators of fluctuating ecological conditions in arctic and subarctic marine ecosystems. We present a high-quality chromosome-level reference genome and annotation for the black-legged kittiwake using a combination of Pacific Biosciences HiFi sequencing, Bionano optical maps, Hi-C reads, and RNA-Seq data. The final assembly spans 1.35 Gb across 32 chromosomes, with a scaffold N50 of 88.21 Mb and a BUSCO completeness of 97.4%. This genome assembly substantially improves the quality of a previous draft genome, showing an approximately 5× increase in contiguity and a more complete annotation. Using this new chromosome-level reference genome and three more chromosome-level assemblies of Charadriiformes, we uncover several lineage-specific chromosome fusions and fissions, but find no shared rearrangements, suggesting that interchromosomal rearrangements have been commonplace throughout the diversification of Charadriiformes. This new high-quality genome assembly will enable population genomic, transcriptomic, and phenotype–genotype association studies in a widely studied sentinel species, which may provide important insights into the impacts of global change on marine systems.

Recent ecotypic differentiation provides unique opportunities to investigate the genomic basis and architecture of local adaptation, while offering insights into how species form and persist. Sockeye salmon (Oncorhynchus nerka) exhibit migratory and resident (“kokanee”) ecotypes, which are further distinguished into shore‐spawning and stream‐spawning reproductive ecotypes. Here, we analysed 36 sockeye (stream‐spawning) and kokanee (stream‐ and shore‐spawning) genomes from a system where they co‐occur and have recent common ancestry (Okanagan Lake/River in British Columbia, Canada) to investigate the genomic basis of reproductive and migratory behaviour. Examination of the genomic landscape of differentiation, differences in allele frequencies and genotype–phenotype associations revealed three main blocks of sequence differentiation on chromosomes 7, 12 and 20, associated with migratory behaviour, spawning location and spawning timing. Structural variants identified in these same areas suggest they could contribute to ecotypic differentiation directly as causal variants or via maintenance of their genomic architecture through recombination suppression mechanisms. Genes in these regions were related to spatial memory and swimming endurance (SYNGAP, TPM3), as well as eye and brain development (including SIX6), potentially associated with differences in migratory behaviour and visual habitats across spawning locations, respectively. Additional genes (GREB1L, ROCK1) identified here have been associated with timing of migration in other salmonids and could explain variation in timing of O. nerka spawning. Together, these results based on the joint analysis of sequence and structural variation represent a significant advance in our understanding of the genomic landscape of ecotypic differentiation at different stages in the speciation continuum.

Background selection (BGS), the effect that purifying selection exerts on sites linked to deleterious alleles, is expected to be ubiquitous across eukaryotic genomes. The effects of BGS reflect the interplay of the rates and fitness effects of deleterious mutations with recombination. A fundamental assumption of BGS models is that recombination rates are invariant over time. However, in some lineages, recombination rates evolve rapidly, violating this central assumption. Here, we investigate how recombination rate evolution affects genetic variation under BGS. We show that recombination rate evolution modifies the effects of BGS in a manner similar to a localized change in the effective population size, potentially leading to underestimation or overestimation of the genome-wide effects of selection. Furthermore, we find evidence that recombination rate evolution in the ancestors of modern house mice may have impacted inferences of the genome-wide effects of selection in that species.

Gene regulatory divergence is thought to play an important role in adaptation, yet its extent and underlying mechanisms remain largely elusive under scenarios of local adaptation with gene flow. Local adaptation is widespread in marine species despite generally high connectivity and often associated with tightly-linked genomic architectures, such as chromosomal inversions. To investigate gene regulatory evolution under gene flow and the role of discrete genomic regions associated with local adaptation to a steep thermal gradient, we generated RNA-seq data from Atlantic silversides ( Menidia menidia ) from two locally adapted populations and their F1 hybrids, reared under two different temperatures. We found substantial divergence in gene expression and thermal plasticity, with up to 31% of genes being differentially expressed, and primarily trans -rather than cis -regulatory divergence between populations, despite ongoing gene flow. Substantially reduced thermal plasticity, temperature-dependent gene misexpression and the disruption of co-expression networks in hybrids point toward a role of regulatory incompatibilities in maintaining local adaptation, particularly under colder temperatures, which appear more challenging for this species. Adaptive chromosomal inversions seem to play an important role in gene regulatory divergence through the accumulation of regulatory incompatibilities but are not consistently enriched for divergently regulated genes. Together, these results highlight that gene regulation can diverge substantially among populations connected by strong gene flow in marine environments, partly due to the accumulation of temperature-dependent regulatory incompatibilities within inversions.