Conservation genomics analysis reveals recent population decline and possible causes in bumblebee Bombus opulentus.

Bumblebees are a genus of pollinators (Bombus) that play important roles in natural ecosystem and agricultural production. Several bumblebee species have been recorded as under population decline, and the proportion of species experiencing population decline within subgenus Thoracobombus is higher than average. Bombus opulentus is 1 species in Thoracobombus, but little is known about its recent population dynamics. Here, we employed conservation genomics methods to investigate the population dynamics of B. opulentus during the recent past and identify the likely environmental factors that may cause population decline. Firstly, we placed the scaffold-level of B. opulentus reference genome sequence onto chromosome-level using Hi-C technique. Then, based on this reference genome and whole-genome resequencing data for 51 B. opulentus samples, we reconstructed the population structure and effective population size (Ne ) trajectories of B. opulentus and identified genes that were under positive selection. Our results revealed that the collected B. opulentus samples could be divided into 2 populations, and 1 of them experienced a recent population decline; the declining population also exhibited lower genetic diversity and higher inbreeding levels. Genes related to high-temperature tolerance, immune response, and detoxication showed signals of positive selection in the declining population, suggesting that climate warming and pathogen/pesticide exposures may contribute to the decline of this B. opulentus population. Taken together, our study provided insights into the demography of B. opulentus populations and highlighted that populations of the same bumblebee species could have contrasting Ne trajectories and population decline could be caused by a combination of various stressors.

Pan-genome analysis highlights the role of structural variation in the evolution and environmental adaptation of Asian honeybees.

The Asian honeybee, Apis cerana, is an ecologically and economically important pollinator. Mapping its genetic variation is key to understanding population-level health, histories and potential capacities to respond to environmental changes. However, most efforts to date were focused on single nucleotide polymorphisms (SNPs) based on a single reference genome, thereby ignoring larger scale genomic variation. We employed long-read sequencing technologies to generate a chromosome-scale reference genome for the ancestral group of A. cerana. Integrating this with 525 resequencing data sets, we constructed the first pan-genome of A. cerana, encompassing almost the entire gene content. We found that 31.32% of genes in the pan-genome were variably present across populations, providing a broad gene pool for environmental adaptation. We identified and characterized structural variations (SVs) and found that they were not closely linked with SNP distributions; however, the formation of SVs was closely associated with transposable elements. Furthermore, phylogenetic analysis using SVs revealed a novel A. cerana ecological group not recoverable from the SNP data. Performing environmental association analysis identified a total of 44 SVs likely to be associated with environmental adaptation. Verification and analysis of one of these, a 330 bp deletion in the Atpalpha gene, indicated that this SV may promote the cold adaptation of A. cerana by altering gene expression. Taken together, our study demonstrates the feasibility and utility of applying pan-genome approaches to map and explore genetic feature variations of honeybee populations, and in particular to examine the role of SVs in the evolution and environmental adaptation of A. cerana.

Conservation Genomic Analysis of the Asian Honeybee in China Reveals Climate Factors Underlying Its Population Decline.

The Asian honeybee, Apis cerana, is one of the most important native pollinators in Asia. Asian honeybees were believed to be under significant decline in China based on a report in 2005. On the contrary, a recent survey revealed that Asian honeybee populations in China are stable and even slightly increased in some regions. Therefore, the declining status of A. cerana populations in China is still unclear. Taking advantage of the abundant, publicly available genomic data for Asian honeybees in China, we employed conservation genomics methods to understand if Asian honeybee populations in China are declining and what the underlying climate factors are. We reconstructed the changes of effective population size (Ne) within the recent past for 6 population groups of Asian honeybees and found out that only one of them (population in Bomi, Tibet) showed a consistently declining Ne from the last 100 generations to 25 generations. Selective sweep analysis suggests that genes related to the tolerance of low temperatures and strong ultraviolet radiation are under selection in the declining population, indicating that these two climate factors most likely underlie the decline of BM populations during the recent past. Our study provides insights into the dynamic changes of Asian honeybee populations in China and identifies climate factors that underlie its population decline, which is valuable for the conservation of this important pollinator.

Genus-Wide Characterization of Nuclear Mitochondrial DNAs in Bumblebee (Hymenoptera: Apidae) Genomes.

In eukaryotes, DNA of mitochondria is transferred into the nucleus and forms nuclear mitochondrial DNAs (NUMTs). Taking advantage of the abundant genomic resources for bumblebees, in this study, we de novo generated mitochondrial genomes (mitogenomes) for 11 bumblebee species. Then, we identified and characterized NUMTs in genus-wide bumblebee species. The number of identified NUMTs varies across those species, with numbers ranging from 32 to 72, and nuclear genome size is not positively related to NUMT number. The insertion sites of NUMTs in the nuclear genome are not random, with AT-rich regions harboring more NUMTs. In addition, our results suggest that NUMTs derived from the mitochondrial COX1 gene are most abundant in the bumblebee nuclear genome. Although the majority of NUMTs are found within intergenic regions, some NUMTs do reside within genic regions. Transcripts that contain both the NUMT sequence and its flanking non-NUMT sequences could be found in the bumblebee transcriptome, suggesting a potential domestication of NUMTs in the bumblebee. Taken together, our results shed light on the molecular features of NUMTs in the bumblebee and uncover their contribution to genome innovation.