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Biology subjects

Atmore, L. M.

Publications and source records attributed to Atmore, L. M..

6 recordsLinked to original sources

Ancient DNA reveals historical demographic decline and genetic erosion in the Atlantic bluefin tuna

Overexploitation has depleted fish stocks during the past century, nonetheless its genomic consequences remain poorly understood. Characterising the spatiotemporal patterns of these consequences may provide baseline estimates of past diversity and productivity to aid management targets, help predict future dynamics, and facilitate the identification of evolutionary factors limiting fish population recovery. Here, we evaluate human impacts on the evolution of the iconic Atlantic bluefin tuna (Thunnus thynnus), one of the longest and most intensely exploited marine fishes, with a tremendous cultural and economic importance. We sequenced whole genomes from modern (n=49) and ancient (n=41) specimens dating up to 5000 years ago, uncovering several novel findings. First, we identify temporally stable patterns of population admixture, as bluefin tuna caught off Norway and in the eastern Mediterranean share a greater degree of ancestry with Gulf of Mexico bluefin tuna than western and central Mediterranean bluefin tuna. This suggests that Atlantic spawning areas are important mixing grounds for the genetic diversity of Mediterranean bluefin tuna. We model effective population size to show that Mediterranean bluefin tuna began to undergo a demographic decline by the year 1900 to an extent not observed across the previous millennia. Coinciding with this, we found that heterozygosity and nucleotide diversity was significantly lower in modern (2013-2020), than ancient (pre-1941) Mediterranean bluefin tuna, suggesting bluefin tuna underwent a genetic bottleneck. With this work we show how ancient DNA provides novel perspectives on ecological complexity with the potential to inform the management and conservation of fishes. SignificanceAchieving the aim of the current UN Ocean Decade to "protect and restore ecosystems and biodiversity" is stymied by a lack of historical knowledge on how human exploitation has impacted and therefore what should be restored. Here, we sequence DNA in ancient fish bones to evaluate the historical diversity of the Atlantic bluefin tuna; which has been of great commercial importance for centuries. We find that bluefin tuna began to undergo demographic decline by 1900, 70 years earlier than currently recognised. Correspondingly, we find modern bluefin tuna had lower levels of genetic diversity than historical ones. This suggests that human impacts on the diversity of marine fishes are likely to have begun earlier and be more complex than previously thought.

ecology↗

The Once and Future Fish: 1300 years of Atlantic herring population structure and demography revealed through ancient DNA and mixed-stock analysis

Atlantic herring populations have been the target of highly profitable coastal and pelagic fisheries in northern Europe for well over a thousand years. Their complex and intermingled population dynamics have sparked extensive debate over the impacts of historical overfishing and have complicated their sustainable management today. Recently developed tools - including diagnostic SNP panels for mixed-stock analysis - aim to improve population assignment for fisheries management, however, the biological relevance of such tools over long periods of time remains unknown. Here, we demonstrate the millennium-long applicability of diagnostic SNP panels and identify population perturbations associated with increasing exploitation pressure and climate change by analyzing whole genome data from modern and ancient herring specimens. We find that herring demographic cycles were likely within healthy ecosystem boundaries until the dramatic disruption of these cycles in the 20th century. We find only autumn-spawning herring in our archaeological remains spanning 900 years from 8 sites across Europe, supporting observations that the numerical dominance of specific spawning populations can demographically outcompete other herring types. We also obtain pre-archival aDNA evidence for the famous, cyclical "Bohuslan periods," during which mass quantities of North Sea autumn-spawning herring congregated in the Skagerrak. Finally, the long-term applicability of diagnostic SNP panels underscores their highly cost-effective application for the genetic monitoring of herring stocks. Our results highlight the utility of ancient DNA and genomic analysis to obtain historical and natural insights in herring ecology and population dynamics with relevance for sustainable fisheries management.

ecology↗

Five millennia of mitochondrial introgression in Atlantic bluefin tuna identified using ancient DNA

Mitogenomic (MT) introgression between species is readily documented in marine fishes. Such introgression events may either be long-term natural phenomena or the result of human-driven shifts in spatial distributions of previously separated species. Determining the drivers behind MT introgression is stymied by the difficulty of directly observing patterns of interbreeding over long timescales. Using ancient DNA spanning five millennia, we here investigate the long-term presence of MT introgression from Pacific bluefin tuna (Thunnus orientalis) and albacore (Thunnus alalunga) into Atlantic bluefin tuna (Thunnus thynnus), a species with extensive exploitation history and observed shifts in abundance, and demographic distribution. Comparing ancient (n=130) and modern (n=78) mitogenomes of specimens covering most of the range of Atlantic bluefin tuna we detect no significant spatial or temporal population structure. This lack of spatiotemporal genomic differentiation is indicative of ongoing gene flow between populations and large effective population sizes over millennia. Moreover, we identify introgressed MT genomes in ancient specimens up to 5000 years old and find that this rate of introgression has remained similar through time. We therefore conclude that MT introgression in the Atlantic bluefin tuna is to date unaffected by anthropogenic impacts. By providing the oldest example of directly observed MT introgression in the marine environment, our results highlight the utility of ancient DNA to obtain temporal insights in the long-term persistence of such phenomena.

evolutionary biology↗

Ancient DNA evidence for the ecological globalisation of cod fishing in medieval and post-medieval Europe

Understanding the historical emergence and growth of long-range fisheries can provide fundamental insights into the timing of ecological impacts and the development of coastal communities during the last millennium. Whole genome sequencing approaches can improve such understanding by determining the origin of archaeological fish specimens that may have been obtained from historic trade or distant water. Here, we used genome-wide data to individually infer the biological source of 37 ancient Atlantic cod specimens (ca. 1050 to 1950 CE) from England and Spain. Our findings provide novel genetic evidence that eleventh- to twelfth-century specimens from London were predominantly obtained from nearby populations, while thirteenth- to fourteenth-century specimens derived from distant sources. Our results further suggest that Icelandic cod was exported to London earlier than previously reported. Our observations confirm the chronology and geography of the trans-Atlantic cod trade from Newfoundland to Spain starting by the early sixteenth century. Our findings demonstrate the utility of whole genome sequencing and ancient DNA approaches to describe the globalisation of marine fisheries and increase our understanding regarding the extent of the North-Atlantic fish trade and long-range fisheries in medieval and early modern times.

ecology↗

Serial depletion of Baltic herring since the Viking Age revealed by ancient DNA and population genomics

Marine resource consumption has been a key component in European diet and culture since the Middle Ages, when fish consumption increased dramatically. Yet, the early origins of marine industries and the long-term ecological consequences of historical and contemporary fisheries remain debated. The Baltic Sea was home to the first "industrial" fishery [~]800 years ago targeting the Baltic herring, a species that is still economically and culturally important today. We combine modern whole genome data with ancient DNA (aDNA) to identify the first known long-distance herring trade in the region, illustrating that large-scale fish trade began during the Viking Age. We resolve population structure within the Baltic and observe demographic independence for four local herring stocks over at least 200 generations. It has been suggested that overfishing at Oresund in the 16th century resulted in a demographic shift from autumn-spawning to spring-spawning herring dominance in the Baltic. We show that while the Oresund fishery had a negative impact on the western Baltic herring stock, the existence of autumn-spawning refugia in other regions of the Baltic delayed the demographic shift to spring spawning dominance until the 20th century. Importantly, modelling demographic trajectories over time, we identify a consistent pattern of serial depletion within the Baltic that is associated with changes in fishing pressure and climate, and conclude that herring exploitation at both historical and recent intensities is not sustainable. Our results highlight the complex and enduring impacts humans have had on the marine environment well before the industrial era.

ecology↗

An accurate assignment test for extremely low-coverage whole-genome sequence data

Genomic assignment tests can provide important diagnostic biological characteristics, such as population of origin or ecotype. In ancient DNA research, such characters can provide further information on population continuity, evolution, climate change, species migration, or trade, depending on archaeological context. Yet, assignment tests often rely on moderate- to high-coverage sequence data, which can be difficult to obtain for many ancient specimens and in ecological studies, which often use sequencing techniques such as ddRAD to bypass the need for costly whole-genome sequencing. We have developed a novel approach that efficiently assigns biologically relevant information (such as population identity or structural variants) 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 from ancient specimens 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 inversion haplotypes and population identity in several species including Heliconius butterflies, Atlantic herring, and Atlantic cod. We used both modern and ancient specimens, including the first whole-genome sequence data recovered from ancient herring bones. The method accurately assigns biological characteristics, including population membership, using extremely low-coverage (e.g. 0.0001x fold) based on genome-wide SNPs. This approach will therefore increase the number of ancient samples in ecological and bioarchaeological research for which relevant biological information can be obtained.

bioinformatics↗