Hans Ellegren’s research while affiliated with Uppsala University and other places

Species-specific sexual traits facilitate species-assortative mating by reducing mating across species and reducing hybrid sexual attractiveness. For learned sexual traits, such as song in oscine birds, species distinctiveness can be eroded when species co-occur. Transcriptional regulatory divergence in brain regions involved in sensory learning are hypothesized to maintain species distinctiveness, but relatively few studies have compared gene expression in relevant brain regions between closely related species. Species differences in song is an important pre-mating reproductive barrier between the collared (Ficedula albicollis) and pied flycatcher (F. hypoleuca). Here, we compare brain gene expression in adult males from each species and their naturally occurring F1 hybrids. We report overall conserved expression across species in a portion of the brain containing regions and nuclei known to be involved in song responses and learning. Further, among those genes that were differentially expressed between species, we find largely intermediate expression in hybrids. A single gene, SYT4 (synaptotagmin 4), known to be singing-associated, both was differentially expressed and has a putative upstream transcriptional regulatory factor containing fixed differences between the two species. Although a finer-scale investigation limited to song-specific regions may reveal further species differences, our findings provide insight into regulatory divergence in the brain between closely related species.

When populations decrease in size and may become isolated, genomic erosion by loss of diversity from genetic drift and accumulation of deleterious mutations is likely an inevitable consequence. In such cases, immigration (genetic rescue) is necessary to restore levels of genetic diversity and counteract inbreeding depression. Recent work in conservation genomics has studied these processes focusing on the genetic diversity of single nucleotide polymorphisms. In contrast, our knowledge about structural genomic variation (insertions, deletions, duplications and inversions) in endangered species is limited. We analysed whole‐genome, short‐read sequences from 212 wolves from the inbred Scandinavian population and from neighbouring populations in Finland and Russia, and detected >35,000 structural variants (SVs) after stringent quality and genotype frequency filtering; >26,000 high‐confidence variants remained after manual curation. The majority of variants were shorter than 1 kb, with a distinct peak in the length distribution of deletions at 190 bp, corresponding to insertion events of SINE/tRNA‐Lys elements. The site frequency spectrum of SVs in protein‐coding regions was significantly shifted towards rare alleles compared to putatively neutral variants, consistent with purifying selection. The realized genetic load of SVs in protein‐coding regions increased with inbreeding levels in the Scandinavian population, but immigration provided a genetic rescue effect by lowering the load and reintroducing ancestral alleles at loci fixed for derived SVs. Our study shows that structural variation comprises a common type of in part deleterious mutations in endangered species and that establishing gene flow is necessary to mitigate the negative consequences of loss of diversity.

Background Reconstructing phylogenetic relationships with genomic data remains a challenging endeavor. Numerous phylogenomic studies have reported incongruent gene trees when analyzing different genomic regions, complicating the search for a ‘true’ species tree. Some authors have argued that genomic regions of increased divergence (i.e. differentiation islands) reflect the species tree, although other studies have shown that these regions might produce misleading topologies due to species-specific selective sweeps or ancient introgression events. In this study, we tested the extent to which highly differentiated loci can resolve phylogenetic relationships in the Bean Goose complex, a group of goose taxa that includes the Taiga Bean Goose ( Anser fabalis ), the Tundra Bean Goose ( Anser serrirostris ) and the Pink-footed Goose ( Anser brachyrhynchus ). Results First, we show that a random selection of genomic loci—which mainly samples the undifferentiated regions of the genome—results in an unresolved species complex with a monophyletic A. brachyrhynchus embedded within a paraphyletic cluster of A. fabalis and A. serrirostris . Next, phylogenetic analyses of differentiation islands converged upon a topology of three monophyletic clades in which A. brachyrhynchus is sister to A. fabalis , and A. serrirostris is sister to the clade uniting these two species. Close inspection of the locus trees within the differentiated regions revealed that this topology was consistently supported over other phylogenetic arrangements. As it seems unlikely that selection or introgression events have impacted all differentiation islands in the same way, we are convinced that this topology reflects the ‘true’ species tree. Additional analyses, based on D-statistics, revealed extensive introgression between A. fabalis and A. serrirostris , which partly explains the failure to resolve the species complex with a random selection of genomic loci. Recent introgression between these taxa has probably erased the phylogenetic branching pattern across a large section of the genome, whereas differentiation islands were unaffected by the homogenizing gene flow and maintained the phylogenetic patterns that reflect the species tree. Conclusions The evolution of the Bean Goose complex can be depicted as a simple bifurcating tree, but this would ignore the impact of introgressive hybridization. Hence, we advocate that the evolutionary relationships between these taxa are best represented as a phylogenetic network.

When new mutations arise at functional sites they are more likely to impair than improve fitness. If not removed by purifying selection, such deleterious mutations will generate a genetic load that can have negative fitness effects in small populations and increase the risk of extinction. This is relevant for the highly inbred Scandinavian wolf (Canis lupus) population, founded by only three wolves in the 1980s and suffering from inbreeding depression. We used functional annotation and evolutionary conservation scores to study deleterious variation in a total of 209 genomes from both the Scandinavian and neighboring wolf populations in northern Europe. The masked load (deleterious mutations in heterozygote state) was highest in Russia and Finland with deleterious alleles segregating at lower frequency than neutral variation. Genetic drift in the Scandinavian population led to the loss of ancestral alleles, fixation of deleterious variants and a significant increase in the per‐individual realized load (deleterious mutations in homozygote state; an increase by 45% in protein‐coding genes) over five generations of inbreeding. Arrival of immigrants gave a temporary genetic rescue effect with ancestral alleles re‐entering the population and thereby shifting deleterious alleles from homozygous into heterozygote genotypes. However, in the absence of permanent connectivity to Finnish and Russian populations, inbreeding has then again led to the exposure of deleterious mutations. These observations provide genome‐wide insight into the magnitude of genetic load and genetic rescue at the molecular level, and in relation to population history. They emphasize the importance of securing gene flow in the management of endangered populations.

Information on genetic population structure provides important knowledge for species conservation. Yet, few studies combine extensive genetic data to evaluate the structure and population dynamics of transboundary populations. Here we used single nucleotide polymorphisms (SNPs), microsatellites and mitochondrial haplotypes to analyze the genetic population structure of wolverines (Gulo gulo) across Fennoscandia using a long-term monitoring dataset of 1708 individuals. Clear population subdivision was detected between the Scandinavian and the eastern Finnish population with a steep cline in the contact zone. While the Scandinavian population showed isolation by distance, large swaths of this population were characterized by high connectivity. Areas with high resistance to gene flow are likely explained by a combination of factors, such as historical isolation and founder effects. From a conservation perspective, promoting gene flow from the population in eastern Finland to the northwest of Scandinavia could augment the less variable Scandinavian population, and increase the demographic resilience of all subpopulations. Overall, the large areas of low resistance to gene flow suggest that transboundary cooperation with aligned actions of harvest and conflict mitigation could improve genetic connectivity across Finland, Sweden, and Norway.

Any random genetic change is more likely to impair than improve fitness, a situation that owes to the fact that contemporary genotypes bear a history of having been shaped by natural selection for a very long time. Most mutations are thus deleterious and generate a genetic load that can be difficult to handle in small populations and increase the risk of extinction. We used functional annotation and evolutionary conservation scores to study deleterious variation in 200+ genomes from the highly inbred Scandinavian wolf population, founded by only three wolves and suffering from inbreeding depression, and neighboring populations in northern Europe. The masked load was high in Russia and Finland with deleterious alleles segregating at lower frequency than neutral variation. Genetic drift in the Scandinavian population led to the loss of ancestral alleles and fixation of deleterious variants. The per-individual realized load increased with the extent of inbreeding and reached several hundred homozygous deleterious genotypes in protein-coding genes, and a total of more than 50,000 homozygous deleterious genotypes in the genome. Arrival of immigrants gave a temporary genetic rescue effect with ancestral alleles re-entering the population and moving deleterious alleles into heterozygote genotypes. However, in the absence of permanent connectivity inbreeding has then again led to the exposure of deleterious mutations. These observations provide genome-wide insight into the character of genetic load and genetic rescue at the molecular level, and in relation to population history. They emphasize the importance of securing gene flow in the management of endangered populations.

Genetic drift can dramatically change allele frequencies in small populations and lead to reduced levels of genetic diversity, including loss of segregating variants. However, there is a shortage of quantitative studies of how genetic diversity changes over time in natural populations, especially on genome-wide scales. Here, we analyzed whole-genome sequences from 76 wolves of a highly inbred Scandinavian population, founded by only one female and two males, sampled over a period of 30 yr. We obtained chromosome-level haplotypes of all three founders and found that 10%–24% of their diploid genomes had become lost after about 20 yr of inbreeding (which approximately corresponds to five generations). Lost haplotypes spanned large genomic regions, as expected from the amount of recombination during this limited time period. Altogether, 160,000 SNP alleles became lost from the population, which may include adaptive variants as well as wild-type alleles masking recessively deleterious alleles. Although not sampled, we could indirectly infer that the two male founders had megabase-sized runs of homozygosity and that all three founders showed significant haplotype sharing, meaning that there were on average only 4.2 unique haplotypes in the six copies of each autosome that the founders brought into the population. This violates the assumption of unrelated founder haplotypes often made in conservation and management of endangered species. Our study provides a novel view of how whole-genome resequencing of temporally stratified samples can be used to visualize and directly quantify the consequences of genetic drift in a small inbred population.

Climate change influences population demography by altering patterns of gene flow and reproductive isolation. Direct mutation rates offer the possibility for accurate dating on the within-species level but are currently only available for a handful of vertebrate species. Here, we use the first directly estimated mutation rate in birds to study the evolutionary history of pied flycatchers ( Ficedula hypoleuca ). Using a combination of demographic inference and species distribution modelling, we show that all major population splits in this forest-dependent system occurred during periods of increased climate instability and rapid global temperature change. We show that the divergent Spanish subspecies originated during the Eemian–Weichselian transition 115–104 thousand years ago (kya), and not during the last glacial maximum (26.5–19 kya), as previously suggested. The magnitude and rates of climate change during the glacial–interglacial transitions that preceded population splits in pied flycatchers were similar to, or exceeded, those predicted to occur in the course of the current, human-induced climate crisis. As such, our results provide a timely reminder of the strong impact that episodes of climate instability and rapid temperature changes can have on species' evolutionary trajectories, with important implications for the natural world in the Anthropocene.

Due to its central importance to many aspects of evolutionary biology and population genetics, the long‐term effective population size (Ne) has been estimated for numerous species and populations. However, estimating contemporary Ne is difficult and in practice this parameter is often not known. In principle, contemporary Ne can be estimated using either analyses of temporal changes in allele frequencies or the extent of linkage disequilibrium (LD) between unlinked markers. We applied these approaches to estimate contemporary Ne of a relatively recently founded island population of collared flycatchers (Ficedula albicollis). We sequenced the genomes of 85 birds sampled in 1993 and 2015, and applied several temporal methods to estimate Ne at a few thousand (4,000 ‐ 7,000). The approach based on LD provided higher estimates of Ne (20,000‐32,000) and were associated with high variance, often resulting in infinite Ne . We conclude that whole‐genome sequence data offer new possibilities to estimate high (>1,000) contemporary Ne, but also note that such estimates remain challenging, in particular for LD‐based methods for contemporary Ne estimation.

A current debate within population genomics surrounds the relevance of patterns of genomic differentiation between closely related species for our understanding of adaptation and speciation. Mounting evidence across many taxa suggests that the same genomic regions repeatedly develop elevated differentiation in independent species pairs. These regions often coincide with high gene density and/or low recombination, leading to the hypothesis that the genomic differentiation landscape mostly reflects a history of background selection, and reveals little about adaptation or speciation. A comparative genomics approach with multiple independent species pairs at a timescale where gene flow and ILS are negligible permits investigating whether different evolutionary processes are responsible for generating lineage‐specific versus shared patterns of species differentiation. We use whole‐genome re‐sequencing data of 195 individuals from four Ficedula flycatcher species comprising two independent species pairs: collared and pied flycatchers, and red‐breasted and taiga flycatchers. We found that both shared and lineage‐specific FST peaks could partially be explained by selective sweeps, with recurrent selection likely to underlie shared signatures of selection, while indirect evidence supports a role of recombination landscape evolution in driving lineage specific‐signatures of selection. This work therefore provides evidence for an interplay of positive selection and recombination to genomic landscape evolution. This article is protected by copyright. All rights reserved