Queens and Workers Contribute Differently to Adaptive Evolution in Bumble Bees and Honey Bees

Harpur, Brock A.; Dey, Alivia; Albert, Jennifer Robin; Patel, Sani; Hines, Heather M.; Hasselmann, Martin; Packer, Laurence; Zayed, Amro

doi:10.1093/gbe/evx182

Cited by 27 publications

(38 citation statements)

References 41 publications

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“…Libraries were aligned to the Bombus impatiens 2.0 genome (Sadd et al., ) using bwa‐mem (Li, ). Bombus impatiens is a close relative of the target species (all Pyrobombus ), and bumble bee genomes have high synteny (Sadd et al., ), so cross‐species mapping performs well (Harpur et al., ; Lozier & Zayed, ). SAM outputs were converted to BAM and sorted with samtools 1.2 (Li et al., ).…”

Section: Methodsmentioning

confidence: 99%

Distance, elevation and environment as drivers of diversity and divergence in bumble bees across latitude and altitude

et al. 2018

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Identifying drivers of dispersal limitation and genetic differentiation is a key goal in biogeography. We examine patterns of population connectivity and genetic diversity using restriction site-associated DNA sequencing (RADseq) in two bumble bee species, Bombus vosnesenskii and Bombus bifarius, across latitude and altitude in mountain ranges from California, Oregon and Washington, U.S.A. Bombus vosnesenskii, which occurs across a broader elevational range at most latitudes, exhibits little population structure while B. bifarius, which occupies a relatively narrow higher elevation niche across most latitudes, exhibits much stronger population differentiation, although gene flow in both species is best explained by isolation with environmental niche resistance. A relationship between elevational habitat breadth and genetic diversity is also apparent, with B. vosnesenskii exhibiting relatively consistent levels of genetic diversity across its range, while B. bifarius has reduced genetic diversity at low latitudes, where it is restricted to high-elevation habitat. The results of this study highlight the importance of the intersect between elevational range and habitat suitability in influencing population connectivity and suggest that future climate warming will have a fragmenting effect even on populations that are presently well connected, as they track their thermal niches upward in montane systems.

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Section: Methodsmentioning

confidence: 99%

Distance, elevation and environment as drivers of diversity and divergence in bumble bees across latitude and altitude

et al. 2018

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“…Moreover, genes related to yolk production, such as vg related genes, are commonly highly expressed in nurses of T. angustula and Apis 4,5,34 , but not in B. terrestris nurses. This is not unexpected since each lineage forgo unique selective pressures, despite presenting similar behaviours 49 . Even closely related species (within the same taxonomic genus) are known to differ in the expression pattern of certain genes 11 .…”

Section: Discussionmentioning

confidence: 78%

Multiple lineages, same molecular basis: task specialization is commonly regulated across all eusocial bee groups

Araujo

Arias

2020

Preprint

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14A striking feature of advanced insect societies is the existence of workers that forgo 15 reproduction. Two broad types of workers exist in eusocial bees: nurses which care 16 for their young siblings and the queen, and foragers who guard the nest and forage for 17 food. Comparisons between this two worker subcastes have been performed in 18 honeybees, but data from other bees are scarce. To understand whether similar 19 molecular mechanisms are involved in nurse-forager differences across distinct 20 species, we compared gene expression and DNA methylation profiles between nurses 21 and foragers of the buff-tailed bumblebee Bombus terrestris and of the stingless bee 22Tetragonisca angustula. These datasets were then discussed comparatively to 23 previous findings on honeybees. Our analyses revealed that although the expression 24 pattern of genes is often species-specific, many of the biological processes and 25 molecular pathways involved are common. Moreover, DNA methylation and gene 26 expression correlation were dependent on the nucleotide context. 27 subcastes evolved it is necessary to differentiate such more recent changes -that 53 could be species-specific -from those shared across species, and thus likely ancestral. 54The highly eusocial stingless bees have age-based division of labour 18 , similarly to 55 that of honeybees despite their most common ancestor being 50 to 80 million years 56 ago 19,20 . To date, no global expression or epigenetic studies have been performed in 57 stingless bees to understand worker task specialization. Similarly, while primitively 58 eusocial bumblebees are largely studied ecological biological models and important 59 wild and managed pollinators, we know comparatively little about the molecular 60 underpinnings of differences between its worker subcastes. Indeed, studies have been 61 restricted to few genes, leaving many open questions [21][22][23] . A major limiting element 62 for these studies is that this species display a somewhat fluctuating division of labour 63 with indistinctive separation between subcastes 10,21,23 . 64We aim to fill in this knowledge gap through the analyses of the global gene 65 expression differences between nurses and foragers, and the characterization of nurses 66 DNA methylation profile in two eusocial bee species, the primitively eusocial buff-67 tailed bumblebee, Bombus terrestris, and the highly eusocial stingless bee, 68Tetragonisca angustula. Combined, these two bee species and the honeybee represent 69 the three evolutionary branches of eusocial corbiculates sharing a common social 70 origin 24 . Hence, in addition to using the generated datasets to uncover unique and 71 more recent molecular traits linked to task division in B. terrestris and T. angustula, 72 we also verified whether common genes and pathways could be involved in task 73 specialization across all the eusocial bee groups. 74 75Results 76 task-dependent foraging gene expression in the bumblebee Bombus terrestris. Arch. Insect

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“…Contrary to our prediction, targets of lineage-specific miRNAs were not significantly enriched for genes under selection in any species. We assessed overlaps between genes undergoing positive directional selection in A. mellifera [53], B. impatiens [54], M. genalis [33], and N. melanderi [32] and the predicted targets of lineage-specific miRNAs in each species. There was no significant enrichment for targets of lineage-specific miRNAs with genes under positive directional selection in any species (Table S4).…”

Section: Resultsmentioning

confidence: 99%

Brain microRNAs among social and solitary bees

Kapheim

Jones

Søvik

et al. 2019

Preprint

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37Evolutionary transitions to a social lifestyle in insects are associated with lineage-specific 38 changes in gene expression, but the key nodes that drive these regulatory changes are largely 39 unknown. We tested the hypothesis that changes in gene regulation associated with social 40 evolution are facilitated by lineage-specific function of microRNAs (miRNAs). Genome scans 41 across 12 bee species showed that miRNA copy-number is mostly conserved and not associated 42 with sociality. However, deep sequencing of small RNAs in six bee species revealed a 43 substantial proportion (20-35%) of detected miRNAs had lineage-specific expression in the 44 brain, 24-72% of which did not have homologs in other species. Lineage-specific miRNAs 45 disproportionately target lineage-specific genes, and have lower expression levels than shared 46 miRNAs. The predicted targets of lineage-specific miRNAs are enriched for genes related to 47 social behavior in social species, but they are not enriched for genes under positive selection. 48Together, these results suggest that novel miRNAs may contribute to lineage-specific patterns of 49 social evolution. Our analyses also support the hypothesis that many new miRNAs are purged by 50 selection due to deleterious effects on mRNA targets, and suggest genome structure is not as 51 influential in regulating bee miRNA evolution as has been shown for mammalian miRNAs. 52 53 specific 55 56 57Eusociality has evolved several times in the hymenopteran insects. In its most basic form, 58 this lifestyle involves reproductive queens living with their worker daughters who forego direct 59 reproduction to cooperatively defend the nest, care for their siblings, and forage for the colony. 60 Due to the complex nature of this lifestyle, the evolution of eusociality likely requires 61 modification of molecular pathways related to development, behavior, neurobiology, physiology, 62 and morphology [1]. The evolution of eusociality is thus expected to involve both genetic 63 changes as well as changes in the way the genome responds to the environment [2]. It is 64therefore unsurprising that recent studies aimed at identifying the genomic signatures of eusocial 65 evolution in insects have found that social species share an increased capacity for gene regulation 66 [3,4]. Evidence for this comes from signatures of rapid evolution of genes involved in 67 transcription and translation, gene family expansions of transcription factors, and increasing 68 potential for DNA methylation and transcription factor binding activity in conserved genes. 69Interestingly, while these types of regulatory changes are common to independent origins and 70 elaborations of eusociality, the specific genes and regulatory elements involved are unique to 71 each lineage [3][4][5]. This suggests that lineage-specific processes are influential in generating new 72 patterns of gene regulation that contribute to social behavior. 73 74 Small, non-coding RNAs such as microRNAs (miRNAs) may be an important source of 75 regulatory novel...

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Queens and Workers Contribute Differently to Adaptive Evolution in Bumble Bees and Honey Bees

Cited by 27 publications

References 41 publications

Distance, elevation and environment as drivers of diversity and divergence in bumble bees across latitude and altitude

Distance, elevation and environment as drivers of diversity and divergence in bumble bees across latitude and altitude

Multiple lineages, same molecular basis: task specialization is commonly regulated across all eusocial bee groups

Brain microRNAs among social and solitary bees

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