Aryn P. Wilder

Global climate change poses a substantial challenge for many species, particularly when habitat loss and fragmentation prevent a species from shifting its range to track suitable climate conditions. Instead, these species must adapt in situ to a different climate environment, making their capacity for adaptation critical to persistence. Yet endangered species often face the added challenge of low standing genetic variation needed for an evolutionary response. Here, we assess adaptive potential in the endangered Pacific pocket mouse ( Perognathus longimembris pacificus ). Using whole-genome sequences spanning nearly a century, we identify 14 candidate genes associated with temperature and moisture, including many with vascular and circulatory functions. Using a reintroduced population, we find more alleles than expected by chance shifted toward the frequencies predicted for the climate of the reintroduction locality. Despite extreme population declines over the past century, these findings indicate that conservation breeding and reintroduction have retained genetic variation relevant to adaptive potential in the Pacific pocket mouse.

Chromosomal inversions are often implicated in divergence between distinct ecotypes, but their role in maintaining continuous adaptive divergence in complex traits remains poorly understood. Using quantitative and population genetics, transcriptomics, and artificial selection experiments, we demonstrate how inversions enable clinal adaptive divergence along a steep environmental gradient despite extensive gene flow in a widely distributed marine fish. We show that three inversions are associated with multiple adaptive traits and harbor the strongest signatures of divergent selection in the genome, implying a crucial adaptive role. These inversions exhibit contrasting selection signatures across latitudes, suggesting that they control distinct aspects of the same complex traits and facilitate adaptation in a modular way to different environmental pressures despite gene flow.

Efforts to recover endangered species often rely on restoring populations to their historical range, yet reestablishing lost genetic variation is challenging when the ancestral genetic landscape is poorly understood. The Pacific pocket mouse (Perognathus longimembris pacificus), a federally endangered heteromyid rodent, has been extirpated from most of its range in coastal southern California. Recovery efforts call for establishing new populations in their historic range through translocation, but the extent to which historical patterns of genetic variation can be recapitulated is unknown. To inform conservation planning, we sequenced whole genomes of historical samples, including individuals from populations that went extinct in the mid-1900s. Phylogenetic analyses revealed that mice from the southernmost extirpated population form a clade with a different subspecies, while populations to the north form a sister clade. These findings support morphological evidence calling for a taxonomic revision, which would modify the definition of the historic range and complicate the interpretation of suitable reintroduction sites. Despite this divergence, D-statistics and demographic models indicate historical gene flow among coastal populations, suggesting that alleles reintroduced to the southern coast may echo ancestral connectivity. Thus, management efforts should consider potential receiver sites that contain suitable habitat within this range as viable for population creation. These results highlight the value of historical genomics in guiding conservation decisions, particularly when taxonomic uncertainty, extirpation, and limited genetic diversity constrain modern management. Although historical baselines often cannot be restored, conservation strategies can leverage genomic insights to enhance future adaptive potential and long-term resilience of threatened species.

Habitat loss and fragmentation are major drivers of biodiversity decline, reducing connectivity among populations and leading to genetic isolation, loss of diversity, increased inbreeding, and reduced fitness. Translocations that promote gene flow by introducing genetically distinct individuals—a process known as genetic rescue—can mitigate these effects by increasing genetic diversity, alleviating inbreeding, and improving adaptive capacity. However, a limited understanding of a population's demographic history, genetic differentiation, and connectivity can hinder the effective application of genetic rescue. We used the Stephens' kangaroo rat (Dipodomys stephensi), a species threatened by habitat loss and fragmentation in southern California, as a model for developing range‐wide genetic management strategies. We analyzed mitochondrial DNA and microsatellite data to investigate genetic structure and estimate both historical and recent demographic patterns, and we used landscape resistance modeling to assess the impacts of natural and anthropogenic barriers on gene flow. Genetic analyses suggest a relatively recent diversification of Stephens' kangaroo rat populations, with higher allelic diversity concentrated in central populations and reduced diversity in isolated northern and southern populations. Although natural geographic features explain much of the genetic structure, landscape resistance models showed that anthropogenic barriers (e.g., roads, development) play a key role in current genetic isolation and are expected to continue driving population differentiation. To guide management, we used population viability simulations to test translocation strategies aimed at reversing genetic erosion. Repeated translocations were far more effective than single events at boosting heterozygosity and population persistence. The frequency and size of translocations were less important than their continued implementation. For very small populations, concurrent habitat restoration to increase carrying capacity was essential to prevent extirpation. Our findings highlight the value of integrating genetic, demographic, and landscape data into conservation planning. This approach is broadly applicable to other species experiencing habitat fragmentation and population isolation.

Two-thirds of Earth’s species have undergone population declines, leaving many vulnerable to genomic erosion and inbreeding depression. Genetic rescue can boost the fitness of small populations, but perceived risks of outbreeding depression can limit its use. We quantified these trade-offs in hundreds of endangered Pacific pocket mice ( Perognathus longimembris pacificus ) by combining whole-genome sequences with fitness data. The impacts of genomic erosion in remnant populations were reversed in an admixed breeding program, suggesting the potential benefits of genetic rescue. However, differences in chromosome numbers increase the risk of genetic incompatibilities. Fitness analyses suggested that although admixed karyotypes may have reduced fertility, non-admixed mice with low heterozygosity and high genetic load had even lower fitness, pointing to a greater risk of extinction if populations remain isolated.

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.

As biodiversity loss outpaces recovery, conservationists are increasingly turning to novel tools for preventing extinction, including cloning and in vitro gametogenesis of biobanked cells. However, restoration of populations can be hindered by low genetic diversity and deleterious genetic load. The persistence of the northern white rhino (Ceratotherium simum cottoni) now depends on the cryopreserved cells of 12 individuals. These banked genomes have higher genetic diversity than southern white rhinos (C. s. simum), a sister subspecies that successfully recovered from a severe bottleneck, but the potential impact of genetic load is unknown. We estimated how demographic history has shaped genome‐wide genetic load in nine northern and 13 southern white rhinos. The bottleneck left southern white rhinos with more fixed and homozygous deleterious alleles and longer runs of homozygosity, whereas northern white rhinos retained more deleterious alleles masked in heterozygosity. To gauge the impact of genetic load on the fitness of a northern white rhino population restored from biobanked cells, we simulated recovery using fitness of southern white rhinos as a benchmark for a viable population. Unlike traditional restoration, cell‐derived founders can be reintroduced in subsequent generations to boost lost genetic diversity and relieve inbreeding. In simulations with repeated reintroduction of founders into a restored population, the fitness cost of genetic load remained lower than that borne by southern white rhinos. Without reintroductions, rapid growth of the restored population (>20–30% per generation) would be needed to maintain comparable fitness. Our results suggest that inbreeding depression from genetic load is not necessarily a barrier to recovery of the northern white rhino and demonstrate how restoration from biobanked cells relieves some constraints of conventional restoration from a limited founder pool. Established conservation methods that protect healthy populations will remain paramount, but emerging technologies hold promise to bolster these tools to combat the extinction crisis.