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Populations can adapt to novel selection pressures through dramatic frequency changes in a few genes of large effect or subtle shifts in many genes of small effect. The latter (polygenic adaptation) is expected to be the primary mode of evolution for many life-history traits but tends to be more difficult to detect than changes in genes of large effect. Atlantic cod (Gadus morhua) were subjected to intense fishing pressure over the twentieth century, leading to abundance crashes and a phenotypic shift toward earlier maturation across many populations. Here, we use spatially replicated temporal genomic data to test for a shared polygenic adaptive response to fishing using methods previously applied to evolve-and-resequence experiments. Cod populations on either side of the Atlantic show covariance in allele frequency change across the genome that are characteristic of recent polygenic adaptation. Using simulations, we demonstrate that the degree of covariance in allele frequency change observed in cod is unlikely to be explained by neutral processes or background selection. As human pressures on wild populations continue to increase, understanding and attributing modes of adaptation using methods similar to those demonstrated here will be important in identifying the capacity for adaptive responses and evolutionary rescue.This article is part of the theme issue ‘Detecting and attributing the causes of biodiversity change: needs, gaps and solutions’.

Peer reviewed: True, Funder: McDonald Institute for Archaeological Research, Mediaeval walrus hunting in Iceland and Greenland-driven by Western European demand for ivory and walrus hide ropes-has been identified as an important pre-modern example of ecological globalization. By contrast, the main origin of walrus ivory destined for eastern European markets, and then onward trade to Asia, is assumed to have been Arctic Russia. Here, we investigate the geographical origin of nine twelfth-century CE walrus specimens discovered in Kyiv, Ukraine-combining archaeological typology (based on chaîne opératoire assessment), ancient DNA (aDNA) and stable isotope analysis. We show that five of seven specimens tested using aDNA can be genetically assigned to a western Greenland origin. Moreover, six of the Kyiv rostra had been sculpted in a way typical of Greenlandic imports to Western Europe, and seven are tentatively consistent with a Greenland origin based on stable isotope analysis. Our results suggest that demand for the products of Norse Greenland's walrus hunt stretched not only to Western Europe but included Ukraine and, by implication given linked trade routes, also Russia, Byzantium and Asia. These observations illuminate the surprising scale of mediaeval ecological globalization and help explain the pressure this process exerted on distant wildlife populations and those who harvested them.

Genomic assignment tests can provide important diagnostic biological characteristics, such as population of origin or ecotype. Yet, assignment tests often rely on moderate- to high-coverage sequence data that can be difficult to obtain for fields such as molecular ecology and ancient DNA. We have developed a novel approach that efficiently assigns biologically relevant information (i.e., population identity or structural variants such as inversions) in extremely low-coverage sequence data. First, we generate databases from existing reference data using a subset of diagnostic single nucleotide polymorphisms (SNPs) associated with a biological characteristic. Low-coverage alignment files are subsequently compared to these databases to ascertain allelic state, yielding a joint probability for each association. To assess the efficacy of this approach, we assigned haplotypes and population identity in Heliconius butterflies, Atlantic herring, and Atlantic cod using chromosomal inversion sites and whole-genome data. We scored both modern and ancient specimens, including the first whole-genome sequence data recovered from ancient Atlantic herring bones. The method accurately assigns biological characteristics, including population membership, using extremely low-coverage data (as low as 0.0001x) based on genome-wide SNPs. This approach will therefore increase the number of samples in evolutionary, ecological and archaeological research for which relevant biological information can be obtained.

Figure S1. Cha��ne op��ratoire typology entailing sets of increasingly elaborate steps used to remove and sculpt medieval walrus rostra found in Greenland and Europe. The Kyiv specimens have been classified using this scheme. Type 1 rostra were only modified by cut marks made during removal from the skull. In type 2, the tusk alveoli were thinned by rough parallel cuts that faceted the surface of each socket. Type 3 rostra also exhibit decorative carving of the nasal aperture. In type 4 the tusk sockets are smoothly rather than roughly facetted and the ventral margin between the tusks is always carved. Fragmentary rostra lacking some information can be attributed to broader categories (e.g. type 2/3). Image reproduced from Figure 2 of Barrett et al. (2020), where it was published open access under the CC BY license (http://creativecommons.org/licenses/by/4.0/). Figure S2. Distribution of medieval European finds of walrus rostra that have been genetically analysed. Potential medieval trade routes are also shown. Mitogenomic clade assignment is indicated for each specimen. Stars mark the locations of control samples from Greenland, Iceland, Finnmark and Svalbard. The modern distributions of the eastern and western genetic clades of Atlantic walrus are shaded. Base map after Barrett et al. (2020) and references therein.

Supplementary Figure S1, S2 and S3 illustrating in-detail the results obtained in this study.

Supplementary Figures and Tables S1, S2 and S3

The importance of the Atlantic walrus ivory trade for the colonization, peak, and collapse of the medieval Norse colonies on Greenland has been extensively debated. Nevertheless, no studies have directly traced medieval European ivory back to distinct Arctic populations of walrus. Analysing the entire mitogenomes of 37 archaeological specimens from Europe, Svalbard, and Greenland, we here discover that Atlantic walrus comprises two monophyletic mitochondrial (MT) clades, which diverged between 23 400 and 251 120 years ago. Our improved genomic resolution allows us to reinterpret the geographical distribution of partial MT data from 306 modern and nineteenth-century specimens, finding that one of these clades was exclusively accessible to Greenlanders. With this discovery, we ascertain the biological origin of 23 archaeological specimens from Europe (most dated between 900 and 1400 CE). These results reveal a significant shift in trade from an early, predominantly eastern source towards a near exclusive representation of Greenland ivory. Our study provides empirical evidence for how this remote Arctic resource was progressively integrated into a medieval pan-European trade network, contributing to both the resilience and vulnerability of Norse Greenland society.

Figure S1. Continuous flow system supplying dispersed crude oil into the exposure tanks at different levels. (PDF 167Â kb)

The feasibility of genome-scale studies from archaeological material remains critically dependent on the ability to access endogenous, authentic DNA. In the majority of cases, this represents a few per cent of the DNA extract, at most. A number of specific pre-extraction protocols for bone powder aimed to improve ancient DNA recovery before library amplification have recently been developed. Here, we test the effects of combining two of such protocols, a bleach wash and a predigestion step, on 12 bone samples of Atlantic cod and domestic horse aged 750-1350 cal. years before present. Using high-throughput sequencing, we show that combined together, bleach wash and predigestion consistently yield DNA libraries with higher endogenous content than either of these methods alone. Additionally, the molecular complexity of these libraries is improved and endogenous DNA templates show larger size distributions. Other library characteristics, such as DNA damage profiles or the composition of microbial communities, are little affected by the pre-extraction protocols. Application of the combined protocol presented in this study will facilitate the genetic analysis of an increasing number of ancient remains and will reduce the cost of whole-genome sequencing.

Adaptation to local conditions is a fundamental process in evolution; however, mechanisms maintaining local adaptation despite high gene flow are still poorly understood. Marine ecosystems provide a wide array of diverse habitats that frequently promote ecological adaptation even in species characterized by strong levels of gene flow. As one example, populations of the marine fish Atlantic cod (Gadus morhua) are highly connected due to immense dispersal capabilities but nevertheless show local adaptation in several key traits. By combining population genomic analyses based on 12K single-nucleotide polymorphisms with larval dispersal patterns inferred using a biophysical ocean model, we show that Atlantic cod individuals residing in sheltered estuarine habitats of Scandinavian fjords mainly belong to offshore oceanic populations with considerable connectivity between these diverse ecosystems. Nevertheless, we also find evidence for discrete fjord populations that are genetically differentiated from offshore populations, indicative of local adaptation, the degree of which appears to be influenced by connectivity. Analyses of the genomic architecture reveal a significant overrepresentation of a large ~5 Mb chromosomal rearrangement in fjord cod, previously proposed to comprise genes critical for the survival at low salinities. This suggests that despite considerable connectivity with offshore populations, local adaptation to fjord environments may be enabled by suppression of recombination in the rearranged region. Our study provides new insights into the potential of local adaptation in high gene flow species within fine geographical scales and highlights the importance of genome architecture in analyses of ecological adaptation. This article is protected by copyright. All rights reserved.

Supplementary figures and tables. (PDF 647 kb)

The search for walruses as a source of ivory –a popular material for making luxury art objects in medieval Europe– played a key role in the historic Scandinavian expansion throughout the Arctic region. Most notably, the colonization, peak and collapse of the medieval Norse colony of Greenland have all been attributed to the proto-globalization of ivory trade. Nevertheless, no studies have directly traced European ivory back to distinct populations of walrus in the Arctic. This limits our understanding of how ivory trade impacted the sustainability of northern societies and the ecology of the species they relied on. Here, we compare the mitogenomes of 27 archaeological walrus specimens from Europe and Greenland (most dated between 900 and 1400 CE) and 10 specimens from Svalbard (dated to the 18thand 19th centuries CE) to partial mitochondrial (MT) data of over 300 modern walruses. We discover two monophyletic mitochondrial clades, one of which is exclusively found in walrus populations of western Greenland and the Canadian Arctic. Investigating the chronology of these clades in our European archaeological remains, we identify a significant shift in resource use from predominantly eastern sources towards a near exclusive representation of walruses from western Greenland. These results provide empirical evidence for the economic importance of walrus for the Norse Greenland settlements and the integration of this remote, western Arctic resource into a medieval pan-European trade network.