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Using environmental DNA to unravel aquatic ecosystem dynamics
Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.ORCID iD: 0000-0003-2001-5077
2024 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Human-induced climate change has led to unprecedented declines in Earth's biodiversity and significant habitat loss. Aquatic ecosystems areespecially at risk, facing pollution, overexploitation, and destruction. Consequently, monitoring biodiversity is critical. Traditional monitoring methods are often low in detection rates, time-consuming, invasive, and harmful to species, which hampers comprehensive biodiversity assessments. Environmental DNA (eDNA) offers a rapid alternative fortaxonomic identification, extracting genetic material from soil, sediments, or water without capturing living organisms, proving useful where traditional methods fall short. However, its integration into aquatic ecology is hampered by unresolved methodological issues.

This thesis demonstrates how eDNA can help reconstruct fish colonization histories in lakes post-glacial retreat. I employed species-specific primers with digital droplet PCR and metagenomic shotgun sequencing on ancient DNA from Holocene lake sediments. My findings show the detectability of DNA from ancient fish populations. However, each method exhibited technical limitations that led to varying degrees offalse negatives and false positive results. Additionally, I examined how Northern pike (Esox Lucius) affects ecological speciation in Europeanwhitefish (Coregonus lavaretus), promoting a shift from insectivorous to piscivorous states, enhancing predator biodiversity and biomass. Dietan alyses of piscivorous birds through digital droplet PCR revealed that smaller whitefish support a larger, more diverse bird community. Finally, I compared two molecular techniques for quantifying bird diets from fecal DNA, finding that metabarcoding with a universal fish primer and digital droplet PCR yielded similar results. This research enhances ourunderstanding of the potential and limitations of molecular tools forspecies identification and aids the integration of eDNA into aquatic ecology.

Place, publisher, year, edition, pages
Umeå: Umeå University, 2024. , p. 24
Keywords [en]
Environmental DNA, ancient DNA, colonization, apex predator, pike, whitefish, piscivorous birds, aquatic ecosystems, metabarcoding, digital droplet PCR
National Category
Ecology
Research subject
biology
Identifiers
URN: urn:nbn:se:umu:diva-224501ISBN: 978-91-8070-412-0 (print)ISBN: 978-91-8070-413-7 (electronic)OAI: oai:DiVA.org:umu-224501DiVA, id: diva2:1858869
Public defence
2024-06-14, KBE303, Stora Hörsalen, KBC-huset, Umeå, 13:00 (English)
Opponent
Supervisors
Available from: 2024-05-24 Created: 2024-05-20 Last updated: 2024-05-21Bibliographically approved
List of papers
1. Estimating species colonization dates using DNA in lake sediment
Open this publication in new window or tab >>Estimating species colonization dates using DNA in lake sediment
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2018 (English)In: Methods in Ecology and Evolution, E-ISSN 2041-210X, Vol. 9, no 3, p. 535-543Article in journal (Refereed) Published
Abstract [en]
  1. Detection of DNA in lake sediments holds promise as a tool to study processes like extinction, colonization, adaptation and evolutionary divergence. However, low concentrations make sediment DNA difficult to detect, leading to high false negative rates. Additionally, contamination could potentially lead to high false positive rates. Careful laboratory procedures can reduce false positive and negative rates, but should not be assumed to completely eliminate them. Therefore, methods are needed that identify potential false positive and negative results, and use this information to judge the plausibility of different interpretations of DNA data from natural archives.
  2. We developed a Bayesian algorithm to infer the colonization history of a species using records of DNA from lake-sediment cores, explicitly labelling some observations as false positive or false negative. We illustrate the method by analysing DNA of whitefish (Coregonus lavaretus L.) from sediment cores covering the past 10,000 years from two central Swedish lakes. We provide the algorithm as an R-script, and the data from this study as example input files.
  3. In one lake, Stora Lögdasjön, where connectivity with the proto-Baltic Sea and the degree of whitefish ecotype differentiation suggested colonization immediately after deglaciation, DNA was indeed successfully recovered and amplified throughout the post-glacial sediment. For this lake, we found no loss of detection probability over time, but a high false negative rate. In the other lake, Hotagen, where connectivity and ecotype differentiation suggested colonization long after deglaciation, DNA was amplified only in the upper part of the sediment, and colonization was estimated at 2,200 bp based on the assumption that successful amplicons represent whitefish presence. Here the earliest amplification represents a false positive with a posterior probability of 41%, which increases the uncertainty in the estimated time of colonization.
  4. Complementing careful laboratory procedures aimed at preventing contamination, our method estimates contamination rates from the data. By combining these results with estimates of false negative rates, our models facilitate unbiased interpretation of data from natural DNA archives.
Place, publisher, year, edition, pages
British Ecological Society, 2018
Keywords
ancient DNA, colonization, Coregonus lavaretus, detection probability, divergence, environmental DNA, lake sediment, population age
National Category
Environmental Sciences
Identifiers
urn:nbn:se:umu:diva-143248 (URN)10.1111/2041-210X.12890 (DOI)000426867600010 ()2-s2.0-85030156606 (Scopus ID)
Funder
Swedish Research Council, 2013-5110
Available from: 2017-12-19 Created: 2017-12-19 Last updated: 2024-05-20Bibliographically approved
2. Fish colonization patterns in central Sweden from dropletdigital PCR and shotgun sequencing of sedimentary DNA
Open this publication in new window or tab >>Fish colonization patterns in central Sweden from dropletdigital PCR and shotgun sequencing of sedimentary DNA
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

The natural establishment of Scandinavian fish populations took place following the lastdeglaciation 9,000 to 12,000 years ago when the retreating ice exposed new habitats. Accessibilityof lakes from the Proto-Baltic sea and the southern freshwater habitats was influenced by theirelevation relative to the post-glacial coastline, with some lakes being unreachable due to migrationbarriers. Long standing hypotheses regarding colonization routes have been formulated based onmodern distribution patterns, knowledge of historic climate variations, and species’ tolerances toenvironmental conditions. These hypotheses have not been tested with other forms of evidencebecause long-term data on past fish histories are limited. In this study, the colonization history ofseveral fish species was investigated using historical data combined with analyses of sedimentaryDNA from Lake Hotagen in central Sweden which is located above the post-glacial coastline.DNA was analyzed with droplet digital PCR (ddPCR) and metagenomic shotgun sequencingapproaches. The ddPCR array used specific primers of seven species known to have beenhistorically present at the lake, and successfully detected 5/7 species in the top 80 cm (~3000 years)of the sediment core where DNA was best preserved. Metagenomics however detected 6/8expected genera in all sediment samples dating back 7000 years. Based on our findings, we inferthat 1) (dd)PCR based methods had too low sensitivity to allow consistent detection of fish inancient samples and 2) metagenomics, while sufficiently sensitive, require expanded databases toincrease granularity across species, especially those who are currently underrepresented. 3) Mostfish species likely colonized lake Hotagen soon after the last deglaciation despite the presence ofmigration barriers.

National Category
Ecology
Research subject
biology
Identifiers
urn:nbn:se:umu:diva-224498 (URN)
Available from: 2024-05-20 Created: 2024-05-20 Last updated: 2024-05-21
3. Apex predator induces predator-rich ecosystem state innorthern lakes
Open this publication in new window or tab >>Apex predator induces predator-rich ecosystem state innorthern lakes
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Large predators are disappearing from ecosystems around the world. If predator speciesfacilitate each other’s existence through niche construction, this development could causecascading predator collapses and reduce ecosystem resilience. However, the importance offacilitation for the assembly and function of predator communities remains poorly understood.Here, we show that a large piscivorous fish, the northern pike (Esox lucius), enables theformation of a numerous and diverse predator community by inducing a dwarf ecotype ofEuropean whitefish (Coregonus lavaretus). Pike increases the standing biomass of prey-sized(<200mm) whitefish with a factor of 12.6, allowing small-gaped fish species (Percafluviatilis, Lota lota, Salvelinus alpinus and Salmo trutta) to go from small-growinggeneralists, to large-growing piscivores. Similarly, a guild of piscivorous birds (Gavia arctica,G. stellata, Sterna paradisaea, S. hirundo, Mergus serrator and M. merganser) shift from amixed diet to relying mainly on whitefish prey in presence of pike. Through this regime shift,the functional piscivore biomass in the non-pike fish community increases with a factor of14.2, and the density- and species richness of piscivorous birds increase with factors of 2.08and 2.16, respectively. Our results demonstrate how feedbacks between presence/absence ofimportant predators and the phenotype of prey may keep complex ecosystems in predator-richor predator-depleted states.

National Category
Ecology
Research subject
biochemical pharmacology; biology
Identifiers
urn:nbn:se:umu:diva-224499 (URN)
Available from: 2024-05-20 Created: 2024-05-20 Last updated: 2024-05-20
4. Consistent findings from ddPCR and metabarcoding analyses of piscivorous bird diets
Open this publication in new window or tab >>Consistent findings from ddPCR and metabarcoding analyses of piscivorous bird diets
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

The diet of apex predators is crucial for addressing fundamental ecological questions. The diets ofpiscivorous birds have traditionally been studied using invasive methods that may be harmful.Consequently, researchers have been compelled to explore alternative options. Molecular toolshave proven effective in discerning dietary preferences of piscivorous birds. In this study, a totalof 151 faecal samples were collected from 6 bird species of lacustrine piscivorous birds occupying36 lakes from 2018 to 2022. Faecal samples were analysed using two molecular methods todetermine the proportion of fish DNA using 1) high-throughput sequencing metabarcoding withthe teleo-2 universal fish primer and 2) a digital droplet PCR array with 7 species-specific newlydesigned primers targeting the most common prey fish species in Scandinavian freshwaterecosystems. The dominant prey species identified by both methods were: whitefish (Coregonuslavaretus), Eurasian perch (Perca fluviatilis) and Eurasian minnow (Phoxinus phoxinus). The twomethods showed a high degree of agreement, suggesting that they both provide accurateassessments of the dietary compositions of bird diets.

National Category
Ecology
Research subject
biology; biology
Identifiers
urn:nbn:se:umu:diva-224500 (URN)
Available from: 2024-05-20 Created: 2024-05-20 Last updated: 2024-05-20

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