A phenotypic, transcriptomic, and genomic characterisation of the response to predicted climate change conditions in overwintering Osmia
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Abstract
Climate change poses substantial challenges to wild bees, particularly through
warmer winters that affect the critical overwintering state of temperate species, a
physiological state characterised by non-feeding and, thus, heavily reliant on reduced
ambient temperatures for limited energy consumption. To characterise the effects
of warmer winters on overwintering mason bees across multiple biological levels,
this thesis integrates physiological experiments with transcriptomics and population
genomics in the two species Osmia bicornis and Osmia cornuta.
In Chapter 1, bees were exposed to field-realistic, elevated overwintering temper-
atures, reflecting two major climate change scenarios outlined by the Intergov-
ernmental Panel on Climate Change (SSP2-4.5 and SSP5-8.5). In both species,
emergence timing advanced by three to six weeks and weight loss increased by 17–
60%, yet survival rates during the experiment were unaffected. These phenotypic
responses demonstrate sensitivity to warming winters with potential fitness costs
through reduced energy reserves at diapause termination and through potential
phenological mismatches.
In Chapter 2, the first chromosome-level genome assembly and annotation for O.
cornuta was generated, and together with a preliminary population genetic dataset, it
was used to reveal low DNA methylation and reduced genetic diversity compared to
social bees and other solitary bees. In addition, the employed long-read sequencing-
based genome generation approach was characterised by cost-effectiveness while
achieving high-quality assembly and annotation results and could, thus, serve as a
guide to other de novo genome assembly efforts in non-model organisms.
In Chapter 3, the molecular responses to increased overwintering temperatures
were characterised through RNA-sequencing of brain tissue sampled from the
physiological experiment across multiple time points (Chapter 1). Both species
exhibited extensive transcriptional reorganisation affecting metabolic pathways,
protein homeostasis, and developmental programmes, with responses highly dy-
namic across time—from several hundred differentially expressed genes after one
week to thousands of genes after seven and fourteen weeks. Genes associated with
oxidative phosphorylation and other metabolic processes shifted from suppression
to activation under prolonged warming, highlighting the importance of accumulated
iiitranscriptomic changes. In addition, large population genomic datasets for both spe-
cies, with male samples from across all of Germany, revealed panmictic population
structure and signatures of recent positive selection among temperature-responsive
genes with species-specific patterns.
Together, these results suggest that while mason bees possess potential to respond
to warming winters through phenotypic and transcriptomic plasticity, fitness costs
might still manifest after overwintering due to increased weight loss and priorit-
isation of metabolic transcriptional programmes over developmental programmes,
suggesting that climate change impacts extend beyond direct mortality. As the two
species investigated exhibited remarkably similar phenotypic and transcriptomic
responses despite differences in selection patterns and two-fold differences in ge-
netic diversity, other related species might harbour a similar potential for plastic
responses to warmer winters. While there were sex differences in the physiological
response to elevated temperatures, there was only very limited evidence of sex
differences in the brain transcriptome response, suggestive of either differences in
post-transcriptional regulation or tissue-specificity of sex differences. This integrat-
ive approach, combining experimental, molecular, and genomic methods, provides
mechanistic understanding of thermal responses necessary for scientifically-informed
conservation of wild bees and their pollination services.