Abstract

Invasive species have led to precipitous declines in biodiversity, especially in island systems. Brown (Rattus norvegicus) and black rats (R. rattus) are among the most invasive animals on the planet, with eradication being the primary tool for established island populations. The need for increased research for defining eradication units and monitoring outcomes has been highlighted as a means to maximize success. Haida Gwaii is an archipelago ~100 km off the northern coast of British Columbia, Canada that hosts globally significant breeding populations of seabirds that are at risk due to invasive rats. Here, we paired sampling of brown (n=287) and black (n=291) rats across the Haida Gwaii archipelago (British Columbia, Canada) with genotyping-by-sequencing (10,770-27,686 SNPs) to investigate patterns of population connectivity and infer levels/direction of gene flow among invasive rat populations in Haida Gwaii. We reconstructed three regional clusters for both species (north, central, south), with proximate populations within regions being largely more related than those that were more distant, consistent with predictions from island biogeography theory. Population assignment of recently detected individuals post-eradication on Faraday, Murchison, and the Bischof Islands revealed all were re-invaders from Lyell Island, rather than being on-island survivors. Based on these results, we identified six eradication units constituting single or clusters of islands that would limit the potential for re-invasion, some of which will need to be combined with biosecurity measures. Overall, our results highlight the importance of targeted research prior to conducting eradications and demonstrates a framework for applying population genomics for guiding invasive species management in island systems.

AbstractAccurate knowledge of geographic ranges and genetic relationships among populations is important when managing a species or population of conservation concern. Along the western coast of Canada, a subspecies of the northern goshawk (Accipiter gentilis laingi) is legally designated as Threatened. The range and distinctness of this form, in comparison to the broadly distributed North American subspecies (Accipiter gentilis atricapillus), is unclear. Given this morphological uncertainty, we analyzed genomic relationships in thousands of single nucleotide polymorphisms identified using genotyping-by-sequencing of high-quality genetic samples. Results revealed a genetically distinct population of northern goshawks on the archipelago of Haida Gwaii and subtle structuring among other North American sampling regions. We then developed genotyping assays for ten loci that are highly differentiated between the two main genetic clusters, allowing inclusion of hundreds of low-quality samples and confirming that the distinct genetic cluster is restricted to Haida Gwaii. As the laingi form was originally described as being based in Haida Gwaii (where the type specimen is from), further morphological analysis may result in this name being restricted to the Haida Gwaii genetic cluster. Regardless of taxonomic treatment, the distinct Haida Gwaii genetic cluster along with the small and declining population size of the Haida Gwaii population suggests a high risk of extinction of an ecologically and genetically distinct form of northern goshawk. Outside of Haida Gwaii, sampling regions along the coast of BC and southeast Alaska (often considered regions inhabited by laingi) show some subtle differentiation from other North American regions. These results will increase the effectiveness of conservation management of northern goshawks in northwestern North America. More broadly, other conservation-related studies of genetic variation may benefit from the two-step approach we employed that first surveys genomic variation using high-quality samples and then genotypes low-quality samples at particularly informative loci.

Islands of Haida Gwaii. name, geology, archipelago, Area, latitude, Length, waterbody, longitude, population, country

Individuals were assigned to ddRAD reference populations using the methods outlined in Rannala and Mountain (1997) as implemented in the program Geneclass2 (Piry et al. 2004). (XLSX)

Abstract

Invasive species management practices often include genetic analyses to better inform decision-making and resource allocation. Yet, past management actions may artificially bias recovered patterns of genetic variation; for example, a population bottleneck caused by contemporary culling may mirror some patterns associated with historical isolation. Here, we aimed to disentangle the impacts of past management activities from natural processes for Sitka black-tailed deer (Odocoileus hemionus sitkensis), an invasive species that has been repeatedly culled on two islands, SGang Gwaay and Reef, within the Haida Gwaii archipelago (Canada). We applied a recently developed Genotyping-in-Thousands by sequencing panel to contemporary (e.g., blood, serum, tissue, muscle, feces) and archived deer samples, the latter collected prior to management activity within the system (c. 1997–1998), which allowed us to contextualize conflicting patterns of isolation and connectivity previously observed on SGang Gwaay and Reef. Successful genotyping (92.6%) and population genetic analysis of 292 individuals at 236 SNPs revealed signals of historical isolation on SGang Gwaay and Reef, provided evidence of a founder effect during initial colonization, and indicated an absence of ongoing gene flow. Furthermore, our spatiotemporal analyses consistently supported a priori predictions associated with bottlenecks within post-cull populations, such as within-island loss of genetic variation, elevated within-island kinship, and increased levels of among-island genetic differentiation. These findings are promising for future management of deer on SGang Gwaay and Reef, suggesting that eradications on these islands may be durable. More broadly, our work highlights the importance of understanding management history before interpreting contemporary population genetic data.

Individuals were assigned following the methods of Rannala and Mountain [53] as implemented in Geneclass2 [54]. (Far/Mur) These samples were collected from Faraday and Murchison Island and grouped into a single unit based on a previous study [25]. Only reference populations with >0 probability of assignment in at least one individual are shown.

AbstractThe root of understanding speciation lies in determining the forces which drive it. In many closely-related species, including Sphyrapicus varius, S. nuchalis, and S. ruber, it is assumed that speciation occurred due to isolation in multiple Pleistocene refugia. We used genetic data from 457 samples at the control region, COI, and CHD1Z to examine rangewide population genetic structure and differentiation amongst these three species across each species’ breeding range. In addition, we modelled these species’ ecological niches for the Holocene (~6,000 ya), Last Glacial Maximum (~22,000 ya), and Last Interglacial (~120,000-140,000 ya) to determine if Pleistocene glaciations could have contributed to allopatric distributions, therefore allowing these groups to differentiate. Population genetic data show a potential Pleistocene refugium in Haida Gwaii, an east-west split among S. varius, and low genetic differentiation within each species. Our control region data show some polyphyly, while COI and CHD1Z data show differentiation among species using composite genotypes. Ecological Niche Modelling shows a large amount of niche overlap at each time period suggesting that S. varius, S. nuchalis, and S. ruber may not have been completely allopatric, and these species likely had repeated intermittent contact. Our data support the growing body of research that suggests differentiation despite gene flow. Usage notesVoucher Specimen DataSource museums and identification numbers for all museum specimens used in study. Museum samples from the Royal British Columbia Museum (RBCM), University of British Columbia (UNBC), Queen’s University (QU), University of Michigan (UMich) Museum of Southwest Biology (MSB), American Museum of Natural History (AMNH), University of Washington Burke Museum (UWBM), Royal Alberta Museum (RABM), Field Museum Natural History (FMNH), New Brunswick Museum (NBM), Canadian Museum of Nature (CMN), Smithsonian (Smith) and Royal Saskatchewan Museum (RSKM).VoucherSpecimenData_Dryad.xlsxGeographic dataCoordinate data for all samples used in study.GeographicData_Dryad.xlsxCladesSNPIndelControl region clades, COI SNPs, and CHD1Z Indel loci for each bird in the study.

Population information.

AbstractBrown rats (Rattus norvegicus) have commensally spread from northern China and Mongolia to become among the most invasive species on the planet. Understanding the proximate source(s) of invasion can inform biosecurity plans and eradication strategies for preventing or mitigating impacts to native biodiversity. The Haida Gwaii archipelago, located off the coast of British Columbia, Canada, is a significant nesting site for 1.5 million seabirds across 12 species, half of which are now threatened by brown rats. Local knowledge points to a European origin in the late 1800’s to early 1900’s, though the true source(s) and firm date(s) of invasion remain unknown. To fill these knowledge gaps, we analyzed genotypic data (16,598 SNPs) for 280 brown rats sampled throughout Haida Gwaii relative to a published global database of potential source populations. Principle component analysis and population assignment tests supported multiple potential invasion sources from Europe and North America. Likewise, demographic modelling best supported two invasions into the islands. The first invasion likely occurred in the early 1900’s into the south-central archipelago from Western Europe followed by a more recent invasion in the early 2000’s from Vancouver, British Columbia, into northern Haida Gwaii. The northern invasion of Haida Gwaii could also be indicative of contemporary gene flow between Haida Gwaii and the mainland, representing a significant biosecurity risk. Our results will inform management strategies for invasive rats in Haida Gwaii, and serve as a guide for studies in other isolated systems worldwide. MethodsHG_GlobalRef_17k.vcf: genotypic data for 582 brown rats (Rattus norvegicus) at 16,598 SNPs originally generated via ddRAD; referred to as "17K" dataset in manuscript HG_GlobalRef_5k. vcf: genotypic data for 582 brown rats (Rattus norvegicus) at 5,000 SNPs originally generated via ddRAD; referred to as "5K" dataset in manuscript

Invasive mammals represent a critical threat to island biodiversity; eradications can result in ecological restoration yet may fail in the absence of key population parameters. Over-browsing by invasive Sitka black-tailed deer (Odocoileus hemionus sitkensis) is causing severe ecological and cultural impacts across the Haida Gwaii archipelago (Canada). Previous eradication attempts demonstrate forest regeneration upon deer removal, but reinvasion reverses conservation gains. Here we use restriction-site associated DNA sequencing (12,947 SNPs) to investigate connectivity and gene flow of invasive deer (n=181) across 15 islands, revealing little structure throughout Haida Gwaii and identifying the large, central island of Moresby (>2,600 km2) as the greatest source of migrants. As a result, the archipelago itself should be considered the primary eradication unit, with the exception of geographically isolated islands like SGang Gwaay. Thus, limiting eradications to isolated islands combi...

AbstractInvasive species management practices often include genetic analyses to better inform decision-making and resource allocation. Yet, past management actions may artificially bias recovered patterns of genetic variation; for example, a population bottleneck caused by contemporary culling may mirror some patterns associated with historical isolation. Here, we aimed to disentangle the impacts of past management activities from natural processes for Sitka black-tailed deer (Odocoileus hemionus sitkensis), an invasive species that has been repeatedly culled on two islands, SGang Gwaay and Reef, within the Haida Gwaii archipelago (Canada). We applied a recently developed Genotyping-in-Thousands by sequencing panel to contemporary (e.g., blood, serum, tissue, muscle, feces) and archived deer samples, the latter collected prior to management activity within the system (c. 1997–1998), which allowed us to contextualize conflicting patterns of isolation and connectivity previously observed on SGang Gwaay and Reef. Successful genotyping (92.6%) and population genetic analysis of 292 individuals at 236 SNPs revealed signals of historical isolation on SGang Gwaay and Reef, provided evidence of a founder effect during initial colonization, and indicated an absence of ongoing gene flow. Furthermore, our spatiotemporal analyses consistently supported a priori predictions associated with bottlenecks within post-cull populations, such as within-island loss of genetic variation, elevated within-island kinship, and increased levels of among-island genetic differentiation. These findings are promising for future management of deer on SGang Gwaay and Reef, suggesting that eradications on these islands may be durable. More broadly, our work highlights the importance of understanding management history before interpreting contemporary population genetic data. MethodsSamples were genotyped using a Genotyping-in-Thousands by sequencing (GTseq; Campbell et al. 2015) panel developed in Burgess et al. (2022; https://doi.org/10.1002/ece3.8993) following the modified protocol therein. Raw data were processed using the GTseq workflow (https://github.com/GTseq). Usage notes236loci_292deer.ped: ped file of genotypic data at 236 SNPs collected via GTseq for 292 deer samples. metadata.csv: text file containing individual metadata for all samples used including sample identifiers, location, year, sex and sample type.