Mette Lillie

DNA methylation is a major component of eukaryotic genomes with an important role in the defence against transposable elements, to transcriptionally silence their activity and prevent transposition. DNA methylation also plays a major role in the regulation of gene expression. This dual role can come into conflict, where DNA methylation in gene regulatory regions becomes perturbed due to transposable element transposition, leading to disruption of gene expression. Here, we describe how this conflict is reflected in DNA methylation patterns in the sand lizard genome where there is recent transposable element activity. Using long-read sequencing technology we show that CpG islands in gene transcriptional start sites are typically hypomethylated and associated with higher gene expression. Outside transcriptional start sites, a majority of CpG islands overlapped transposable elements and were associated with hypermethylation, consistent with a host defence role in suppressing transposition activity. We identify 605 instances where transcriptional start sites were associated with transposable elements (4.3% of all genes). These instances were far rarer in conjunction with a CpG island, when methylation signatures would be in conflict. Transposable elements were found to be closer to and at higher density, the more hypermethylated a transcriptional start site was, suggesting strong selection against selfish genetic elements transposing into hypomethylated transcriptional start sites.

Conservation interventions are increasingly required for species threatened by population declines and isolation due to anthropogenic pressures. Small, isolated populations are particularly vulnerable to the loss of genetic diversity, increased inbreeding, and the accumulation of deleterious mutations. Translocations or supplementation of allopatric individuals for genetic rescue may be the only way to increase genetic diversity and increase population persistence via increased adaptive potential. Here, we use an experimentally admixed population of sand lizards on a small island in Sweden as a valuable model of genetic rescue. This population was established approximately 20 years ago (5–6 generations), resulting in increased fecundity and hatchling viability. This population was founded from crossings between individuals from an inbred population from the nearby mainland and individuals sourced from populations in southern Sweden. Low-coverage whole-genome sequencing revealed elevated genetic diversity and reduced realized genetic load in this admixed population relative to the source populations. Ancestry analyses indicated a greater contribution of southern Swedish genetic variation, potentially reflecting the contribution of beneficial adaptive variation from this region that may underlie the positive population effects. This system provides valuable empirical insights into the long-term genomic consequences of genetic rescue in this model vertebrate population.

Conservation interventions are increasingly required for species threatened by population declines and isolation due to anthropogenic pressures. Small, isolated populations are particularly vulnerable to the loss of genetic diversity, increased inbreeding, and the accumulation of deleterious mutations. Translocations or supplementation of allopatric individuals for genetic rescue may be the only way to increase genetic diversity to increase population persistence via increased adaptive potential. Here, we use an experimentally admixed population of sand lizards on a small island in Sweden as a valuable model of genetic rescue. This population was established approximately 20 years ago (5-6 generations) resulting in increased fecundity and hatchling viability. This population was founded from crossings between individuals from an inbred population from the nearby mainland and individuals sourced from populations in southern Sweden. Low-coverage whole-genome sequencing revealed elevated genetic diversity and reduced realized genetic load in this admixed population relative to the source populations. Ancestry analyses indicated a greater contribution of southern Swedish genetic variation, potentially reflecting contribution of beneficial adaptive variation from this region that may underlie the positive population effects. This system provides valuable empirical insights into the long-term genomic consequences of genetic rescue in this model vertebrate population.

Genomics has emerged as a powerful tool in conservation biology, offering valuable insights into the genetic diversity, population connectivity and adaptive potential of threatened species. Here, we apply a large-scale, low-coverage whole genome sequencing approach to the conservation genomics of the Swedish sand lizard (Lacerta agilis). Sand lizards occur in fragmented populations across Sweden, with varying population sizes and degrees of isolation, and face significant threats from habitat degradation and land use change. In this study, we sequenced 139 individuals to investigate genetic diversity, population structure and genetic load. We reveal strong population structure among Swedish sand lizards and identify populations with low genetic diversity and realised high genetic load. Genetic diversity in populations declined with increasing latitude, likely reflecting the historical northward expansion process and the subsequent population fragmentation and isolation. We observe strong population structure and reveal genetic distinctiveness of populations; findings with significant conservation implications. For example, the Sörmon population, a relict population in central Sweden, appears genetically distinct from all other populations. Further, the northern-most populations in Dalarna appear relatively small, with high genetic load, and thus may require intensive management via e.g., restored open successional habitat to aid population recovery. Our study adds to the growing field of conservation genomics and demonstrates the value of high-resolution whole genome approaches to the conservation efforts for threatened populations. Finally, our research contributes crucial insights for the conservation management of this vulnerable species in Sweden.

Koalas (Phascolarctos cinereus) have experienced a history of retroviral epidemics leaving their trace as heritable endogenous retroviruses (ERVs) in their genomes. A recently identified ERV lineage, named phaCin-β, shows a pattern of recent, possibly current, activity with high insertional polymorphism in the population. Here, we investigate geographic patterns of three focal ERV lineages of increasing estimated ages, from the koala retrovirus (KoRV) to phaCin-β and to phaCin-β-like, using the whole-genome sequencing of 430 koalas from the Koala Genome Survey. Thousands of ERV loci were found across the population, with contrasting patterns of polymorphism. Northern individuals had thousands of KoRV integrations and hundreds of phaCin-β ERVs. In contrast, southern individuals had higher phaCin-β frequencies, possibly reflecting more recent activity and a founder effect. Overall, our findings suggest high ERV burden in koalas, reflecting historic retrovirus-host interactions. Importantly, the ERV catalogue supplies improved markers for conservation genetics in this endangered species.

Koalas ( Phascolarctos cinereus ) are subject to retroviral infections by the koala retrovirus (KoRV), resulting in accumulation of heritable endogenous KoRV in the koala germline. Like other vertebrates, koalas have experienced a history of retroviral epidemics leaving marks as endogenous retroviruses (ERVs) in their genomes; another recently identified ERV lineage, named phaCin-β , shows a pattern of recent, possibly current, activity with high insertional polymorphism in the koala population that predates the establishment of endogenous KoRV. We investigate geographic patterns of retrovirus activity, focusing on three distinct ERV lineages of increasing estimated ages from KoRV to phaCin-β and to phaCin-β-like , using a whole-genome sequencing dataset of 430 koalas produced by the Koala Genome Survey. We find thousands of ERV loci across the koala population and identify contrasting patterns of polymorphism. In the youngest established ERV-lineage (KoRV), we identify thousands of integrations among northern individuals. In the phaCin-β ERV lineage, which is slightly older yet with overlapping time of activity with KoRV, we observe hundreds of integrations in northern individuals. In southern koalas, however, phaCin-β loci are found at higher frequencies possibly reflecting a bottleneck effect. Overall, the findings suggest high ERV burden in koalas that represent historic retrovirus-host interactions. Importantly, the ERV catalogue supplies improved markers for population conservation genetics of this endangered species.

Endogenous retroviruses (ERVs) are inherited remnants of retroviruses that colonized host germline over millions of years, providing a sampling of retroviral diversity across time. Here, we utilize the strength of Darwin’s finches, a system synonymous with evolutionary studies, for investigating ERV history, revealing recent retrovirus-host interactions in natural populations. By mapping ERV variation across all species of Darwin’s finches and comparing with outgroup species, we highlight geographical and historical patterns of retrovirus-host occurrence, utilizing the system for evaluating the extent and timing of retroviral activity in hosts undergoing adaptive radiation and colonization of new environments. We find shared ERVs among all samples indicating retrovirus-host associations pre-dating host speciation, as well as considerable ERV variation across populations of the entire Darwin’s finches’ radiation. Unexpected ERV variation in finch species on different islands suggests historical changes in gene flow and selection. Non-random distribution of ERVs along and between chromosomes, and across finch species, suggests association between ERV accumulation and the rapid speciation of Darwin’s finches.

Retroviruses have left their legacy in host genomes over millions of years as endogenous retroviruses (ERVs), and their structure, diversity, and prevalence provide insights into the historical dynamics of retrovirus–host interactions. In bioinformatic analyses of koala ( Phascolarctos cinereus ) whole-genome sequences, we identify a recently expanded ERV lineage ( phaCin-β ) that is related to the New World squirrel monkey retrovirus. This ERV expansion shares many parallels with the ongoing koala retrovirus (KoRV) invasion of the koala genome, including highly similar and mostly intact sequences, and polymorphic ERV loci in the sampled koala population. The recent phaCin-β ERV colonization of the koala genome appears to predate the current KoRV invasion, but polymorphic ERVs and divergence comparisons between these two lineages predict a currently uncharacterized, possibly still extant, phaCin-β retrovirus. The genomics approach to ERV-guided discovery of novel retroviruses in host species provides a strong incentive to search for phaCin-β retroviruses in the Australasian fauna.

Endogenous retroviruses (ERVs) are inherited remnants of past retroviruses that colonized host germline over millions of years, providing a sampling of retroviral diversity across time. The utility of ERVs as markers of host genome evolution is augmented by their ability to reveal historic retrovirus-host interactions, given that ERVs are examples of active retroviruses at the time of germline invasion. Here, we utilize the strength of Darwin’s finches, a system synonymous with evolutionary studies, for investigating ERV history, revealing recent retrovirus-host interactions in natural populations. By mapping ERV variation across all species of Darwin’s finches and comparing with outgroup species, we highlight geographical and historical patterns of retrovirus-host occurrence, utilizing the system as a natural model for evaluating the extent and timing of retroviral activity in hosts undergoing adaptive radiation and colonization of new environments. We found shared ERVs among all samples indicating retrovirus-host associations pre-dating host speciation, as well as considerable ERV variation across populations of the entire Darwin’s finches’ radiation. Unexpected ERV variation in finch species on different islands suggest historical changes in gene flow and selection. Non-random distribution of ERVs along and between chromosomes, as well as across finch species, suggests association between ERV accumulation and the rapid speciation of Darwin’s finches.

The use of genetic markers in the context of conservation is largely being outcompeted by whole-genome data. Comparative studies between the two are sparse, and the knowledge about potential effects of this methodology shift is limited. Here, we used whole-genome sequencing data to assess the genetic status of peripheral populations of the wels catfish (Silurus glanis), and discuss the results in light of a recent microsatellite study of the same populations. The Swedish populations of the wels catfish have suffered from severe declines during the last centuries and persists in only a few isolated water systems. Fragmented populations generally are at greater risk of extinction, for example due to loss of genetic diversity, and may thus require conservation actions. We sequenced individuals from the three remaining native populations (Båven, Emån, and Möckeln) and one reintroduced population of admixed origin (Helge å), and found that genetic diversity was highest in Emån but low overall, with strong differentiation among the populations. No signature of recent inbreeding was found, but a considerable number of short runs of homozygosity were present in all populations, likely linked to historically small population sizes and bottleneck events. Genetic substructure within any of the native populations was at best weak. Individuals from the admixed population Helge å shared most genetic ancestry with the Båven population (72%). Our results are largely in agreement with the microsatellite study, and stresses the need to protect these isolated populations at the northern edge of the distribution of the species.