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Understanding the adaptive capacity of the bumblebee Bombus terrestris across native and novel environments

Hjort, Cecilia LU (2024)
Abstract
Anthropogenic stressors such as agricultural intensification, climate change, andincreased densities of non-native managed bees used for crop pollination arecontributing to bee declines. Understanding how and why bees have responded topast environmental changes is crucial for predicting future ones and enablingmitigation to maintain the functioning of both natural and agricultural ecosystems.The anthropogenic stressors are expected to put demand on the ability of bees torespond to future change. Thus, the ability of bee populations to persist in aparticular area may require adaptive responses via either phenotypic plasticity orevolutionary adaptations in functional traits (e.g. physiological, morphological, andlife-history traits).... (More)
Anthropogenic stressors such as agricultural intensification, climate change, andincreased densities of non-native managed bees used for crop pollination arecontributing to bee declines. Understanding how and why bees have responded topast environmental changes is crucial for predicting future ones and enablingmitigation to maintain the functioning of both natural and agricultural ecosystems.The anthropogenic stressors are expected to put demand on the ability of bees torespond to future change. Thus, the ability of bee populations to persist in aparticular area may require adaptive responses via either phenotypic plasticity orevolutionary adaptations in functional traits (e.g. physiological, morphological, andlife-history traits). However, for bumblebees, it is not fully understood how geneflow and environmental differences affect such adaptations. In this thesis, I studiedthe bumblebee Bombus terrestris in a native (Sweden) and novel (Tasmania,Australia) setting, aiming to investigate: (1) if the introduction of commercial B.terrestris of a different sub-species affects wild Swedish B. terrestris viaintrogressive hybridization using whole-genome sequencing (WGS), and what theevolutionary consequences are; (2) if wild native B. terrestris in Sweden isgenetically structured and shows selection signatures in relation to land use andclimate variables, using double digest restriction-site associated DNA (ddRAD)sequencing; (3) if the recently introduced B. terrestris in Tasmania showsmorphological variation in relation to the island’s heterogeneous environment andclimate, facilitating its invasion success; and finally, (4) if there is evidence forselection on functional genes and morphology in B. terrestris given the novelenvironmental and climatic conditions across Tasmania, using RADseq. From thesefour chapters, I outline several interesting key findings. In Chapter I, I foundgenomic differences between wild Swedish and commercial B. terrestris but noevidence for recent genomic introgression between the two even though feralcommercial bumblebees were present in the wild. Although, non-native B. terrestrisare likely ill-adapted to the Swedish environment but may under future climatechange be able to persist and mate. Chapter II showed that wild B. terrestris in anative range consists mainly of a homogeneous population, but with evidence forweak genetic structuring, separating southern Sweden from the central and morenorthern regions. Our results showed no evidence for signatures of adaptation toagricultural landscape simplification (i.e. the proportion of semi-natural habitat andthe length of uncultivated agricultural field borders). Instead, weak, local geneticadaptation was documented in genes related to insecticide resistance and immune response and associated with higher proportions of agricultural cover and latitudeof sites. Range expansion of B. terrestris was evident via negative Tajima’s D,suggestively in a northward direction and more inland into densely forested areas asevidenced by more recent observational data. We suggest that the species’ generalistand mobile characteristics allow B. terrestris to exploit various environments withlimited genetic local adaptation and suggest this generalist species may not be asseverely affected by land-use change as more specialist bumblebees. In contrast,Chapters III and IV show how B. terrestris in its novel range has locally adaptedto the selection pressures of a novel heterogeneous environment in Tasmania,Australia, specifically to precipitation and wind. Candidate loci found wereannotated to genes involved in cuticle differentiation and cuticle-regulated waterloss prevention, immune response, olfactory system, functions relating to flightmuscles, and fatty acid metabolism. Our results shed further light on how B.terrestris successfully colonized and invaded Tasmania despite the geneticconsequences of a founding bottleneck. Taken together, the four chapters in thisthesis demonstrate how the generalist bumblebee B. terrestris in both its native andinvasive ranges is able to thrive in the face of anthropogenic change and novelheterogeneous environments. This thesis is a testament to the capacity of B.terrestris to be a successful pollinator in native ranges while also being one of theworld’s most successful invasive bee species. (Less)
Please use this url to cite or link to this publication:
author
supervisor
opponent
  • Dr. Carvell, Claire, UK Centre for Ecology & Hydrology
organization
alternative title
Den mörka jordhumlans anpassningsförmåga i inhemska och nya utbredningsområden
publishing date
type
Thesis
publication status
published
subject
keywords
Bumblebees, Bombus terrestris, Pollination, Introgression, Single nucleotide polymorphisms, Whole Genome Sequencing, Landscape simplification, Gene flow, Morphology, Environmental variation, Invasion, Local adaptation, Island
pages
192 pages
publisher
Biologiska institutionen, Lunds universitet
defense location
Blå Hallen, Ekologihuset.
defense date
2024-03-01 09:30:00
ISBN
978-91-8039-923-4
978-91-8039-922-7
language
English
LU publication?
yes
id
fe6a7644-3d8d-481a-b762-390e69cf16d2
date added to LUP
2024-02-05 13:38:53
date last changed
2024-02-07 10:12:42
@phdthesis{fe6a7644-3d8d-481a-b762-390e69cf16d2,
  abstract     = {{Anthropogenic stressors such as agricultural intensification, climate change, andincreased densities of non-native managed bees used for crop pollination arecontributing to bee declines. Understanding how and why bees have responded topast environmental changes is crucial for predicting future ones and enablingmitigation to maintain the functioning of both natural and agricultural ecosystems.The anthropogenic stressors are expected to put demand on the ability of bees torespond to future change. Thus, the ability of bee populations to persist in aparticular area may require adaptive responses via either phenotypic plasticity orevolutionary adaptations in functional traits (e.g. physiological, morphological, andlife-history traits). However, for bumblebees, it is not fully understood how geneflow and environmental differences affect such adaptations. In this thesis, I studiedthe bumblebee Bombus terrestris in a native (Sweden) and novel (Tasmania,Australia) setting, aiming to investigate: (1) if the introduction of commercial B.terrestris of a different sub-species affects wild Swedish B. terrestris viaintrogressive hybridization using whole-genome sequencing (WGS), and what theevolutionary consequences are; (2) if wild native B. terrestris in Sweden isgenetically structured and shows selection signatures in relation to land use andclimate variables, using double digest restriction-site associated DNA (ddRAD)sequencing; (3) if the recently introduced B. terrestris in Tasmania showsmorphological variation in relation to the island’s heterogeneous environment andclimate, facilitating its invasion success; and finally, (4) if there is evidence forselection on functional genes and morphology in B. terrestris given the novelenvironmental and climatic conditions across Tasmania, using RADseq. From thesefour chapters, I outline several interesting key findings. In Chapter I, I foundgenomic differences between wild Swedish and commercial B. terrestris but noevidence for recent genomic introgression between the two even though feralcommercial bumblebees were present in the wild. Although, non-native B. terrestrisare likely ill-adapted to the Swedish environment but may under future climatechange be able to persist and mate. Chapter II showed that wild B. terrestris in anative range consists mainly of a homogeneous population, but with evidence forweak genetic structuring, separating southern Sweden from the central and morenorthern regions. Our results showed no evidence for signatures of adaptation toagricultural landscape simplification (i.e. the proportion of semi-natural habitat andthe length of uncultivated agricultural field borders). Instead, weak, local geneticadaptation was documented in genes related to insecticide resistance and immune response and associated with higher proportions of agricultural cover and latitudeof sites. Range expansion of B. terrestris was evident via negative Tajima’s D,suggestively in a northward direction and more inland into densely forested areas asevidenced by more recent observational data. We suggest that the species’ generalistand mobile characteristics allow B. terrestris to exploit various environments withlimited genetic local adaptation and suggest this generalist species may not be asseverely affected by land-use change as more specialist bumblebees. In contrast,Chapters III and IV show how B. terrestris in its novel range has locally adaptedto the selection pressures of a novel heterogeneous environment in Tasmania,Australia, specifically to precipitation and wind. Candidate loci found wereannotated to genes involved in cuticle differentiation and cuticle-regulated waterloss prevention, immune response, olfactory system, functions relating to flightmuscles, and fatty acid metabolism. Our results shed further light on how B.terrestris successfully colonized and invaded Tasmania despite the geneticconsequences of a founding bottleneck. Taken together, the four chapters in thisthesis demonstrate how the generalist bumblebee B. terrestris in both its native andinvasive ranges is able to thrive in the face of anthropogenic change and novelheterogeneous environments. This thesis is a testament to the capacity of B.terrestris to be a successful pollinator in native ranges while also being one of theworld’s most successful invasive bee species.}},
  author       = {{Hjort, Cecilia}},
  isbn         = {{978-91-8039-923-4}},
  keywords     = {{Bumblebees; Bombus terrestris; Pollination; Introgression; Single nucleotide polymorphisms; Whole Genome Sequencing; Landscape simplification; Gene flow; Morphology; Environmental variation; Invasion; Local adaptation; Island}},
  language     = {{eng}},
  month        = {{02}},
  publisher    = {{Biologiska institutionen, Lunds universitet}},
  school       = {{Lund University}},
  title        = {{Understanding the adaptive capacity of the bumblebee <i>Bombus terrestris </i>across native and novel environments}},
  url          = {{https://lup.lub.lu.se/search/files/170853023/Avhandling_Cecilia_Hjort_utan_papers.pdf}},
  year         = {{2024}},
}