Feminizer and doublesex knock-outs cause honey bees to switch sexes

McAfee, Alison; Pettis, Jeffery S.; Foster, Leonard J.

doi:10.1371/journal.pbio.3000256

Cited by 21 publications

(20 citation statements)

References 18 publications

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“…For example, CRISPR has recently been used to knockout two sex‐determining genes in A. mellifera causing individuals to change gender (Mcafee et al. ). This technology has also been adapted to be able to change the methylation state of a given loci (Vojta et al.…”

Section: Discussionmentioning

confidence: 99%

“…Future work should focus on the consequences of experimental methylation removal or addition (Pegoraro et al 2017), as well as exploring additional epigenetic mechanisms to attempt to identify a full pathway leading to reproductive caste differences. For example, CRISPR has recently been used to knockout two sex-determining genes in A. mellifera causing individuals to change gender (Mcafee et al 2019). This technology has also been adapted to be able to change the methylation state of a given loci (Vojta et al 2016), allowing the possibility of exploring the function of methylation in specific genes.…”

Section: Discussionmentioning

confidence: 99%

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Methylation and gene expression differences between reproductive and sterile bumblebee workers

2019

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Phenotypic plasticity is the production of multiple phenotypes from a single genome and is notably observed in social insects. Multiple epigenetic mechanisms have been associated with social insect plasticity, with DNA methylation being explored to the greatest extent. DNA methylation is thought to play a role in caste determination in Apis mellifera, and other social insects, but there is limited knowledge on its role in other bee species. In this study, we analyzed whole genome bisulfite sequencing and RNA‐seq data sets from head tissue of reproductive and sterile castes of the eusocial bumblebee Bombus terrestris. We found that genome‐wide methylation in B. terrestris is similar to other holometabolous insects and does not differ between reproductive castes. We did, however, find differentially methylated genes between castes, which are enriched for multiple biological processes including reproduction. However, we found no relationship between differential methylation and differential gene expression or differential exon usage between castes. Our results also indicate high intercolony variation in methylation. These findings suggest that methylation is associated with caste differences but may serve an alternate function, other than direct caste determination in this species. This study provides the first insights into the nature of a bumblebee caste‐specific methylome as well as its interaction with gene expression and caste‐specific alternative splicing, providing greater understanding of the role of methylation in phenotypic plasticity within social bee species. Future experimental work is needed to determine the function of methylation and other epigenetic mechanisms in insects.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Methylation and gene expression differences between reproductive and sterile bumblebee workers

2019

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“…The accession for HSP70 is NP_001153536.1. Bee silhouettes are adapted from McAfee et al (2019) 84 (CC-BY 4.0).…”

Section: Resultsmentioning

confidence: 99%

Honey bee queens are vulnerable to heat-induced loss of fertility

McAfee

Chapman

Higo

et al. 2019

Preprint

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13All species need to reproduce to maintain viable populations, but heat stress kills sperm cells across the 14 animal kingdom and rising frequencies of heatwaves are a threat to biodiversity. Honey bees (Apis 15 mellifera) are globally distributed micro-livestock; therefore, they could serve as environmental 16 biomonitors for heat-induced reductions in fertility. Here, we found that queens have two potential 17 routes of temperature-stress exposure: within colonies and during routine shipping. Our data suggest 18 that temperatures of 15 to 38°C are safe for queens at a tolerance threshold of 11.5% loss of sperm 19 viability, which is the viability difference between failed and healthy queens collected from beekeepers. 20Heat shock activates expression of specific ATP-independent heat-shock proteins in the spermatheca, 21 which could serve as biomarkers for heat stress. This protein fingerprint may eventually enable surveys 22 with colony losses 41 . Furthermore, internal hive temperatures positively correlate with ambient 46 temperatures above 18°C, and brood nest temperatures can rise upwards of 37°C, both under natural 47 conditions 42 and during simulated heatwaves 43 . Hives occasionally experience spikes of > 40°C 44 , 48 suggesting that queens could be vulnerable to temperature extremes even inside the hive. 49Honey bees have excellent potential for being temperature stress biomonitors. They are a globally 50 distributed, managed species, so they are readily available in almost any geographic region, and they are 51 already accepted as effective biomonitors for pollution 45 . If we begin to observe signs of heat stress in 52 honey bees colonies, that would signal a worrisome risk of reduced reproductive output for ectothermic 53 species. 54Here, we begin to explore honey bees' utility as temperature stress biomonitors. We monitored 55 temperature fluctuations in colonies under extreme weather conditions, establishing that damaging 56 intra-hive temperatures can occur. Next, we tested a range of temperatures and exposure durations to 57 determine thresholds above which queen quality is likely to be compromised. We then investigated the 58 biochemical basis of heat-induced sperm viability reduction in queens and drones using quantitative 59 proteomics, which showed how heat stress alters protein expression of reproductive tissues. The 60 specific set of upregulated proteins we identified may eventually serve as diagnostic tools to elucidate 61 causes of queen failure and eventually enable regional surveys of heat stress as part of an 62 environmental temperature biomonitoring program. 63 Results and Discussion 64 Stored sperm viability of failed and healthy queens 65To establish how much of a reduction in sperm viability is associated with field-observable reduced 66 reproductive output (and associated economic losses for beekeepers), we collected queens rated as 67 'failing' (N = 58) and 'healthy' (N = 55) by beekeepers and measured the queens' stored sperm viability 68

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“…These proteins determine male and female development, respectively. The function of dsx has been explored in several insects, including Drosophila (Shirangi et al, 2016), beetles (Ledón-Rettig et al, 2017), Bombyx mori (Xu et al, 2017), A. gambiae (Kyrou et al, 2018), and honey bees (McAfee et al, 2019). Previous studies have suggested that lncRNAs can regulate neighboring coding genes (Villegas and Zaphiropoulos, 2015).…”

Section: Discussionmentioning

confidence: 99%

Differentiation of Long Non-Coding RNA and mRNA Expression Profiles in Male and Female Aedes albopictus

Dong

et al. 2019

Front. Genet.

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The Asia tiger mosquito (Aedes albopictus) is an important vector of arboviruses, and females can transmit pathogens such as the dengue, zika, and chikungunya viruses. Understanding sex-related differences in this mosquito is fundamental for vector control. However, there are no reports of systematic characterization of long non-coding RNAs (lncRNAs) in male and female Ae. albopictus. To investigate the roles of coding and non-coding RNAs in both sexes of Ae. albopictus, RNA sequencing was performed on male and female samples. The results showed 305 differentially expressed protein-coding genes (DEGs) between males and females, of which 198 were highly expressed in males and 125 were highly expressed in females. Sex-associated gene ontology terms were enriched. Analysis with the FEELnc software identified 2,623 novel lncRNAs, of which 26 showed male high expression and 11 showed female high expression. Quantitative real-time PCR of randomly selected DEGs and lncRNAs supported the validity of the RNA sequencing results. Knocking down male high-expressed gene AALF000433 in male adults reduced the egg hatching rate. This study provides valuable data on sex-specific expression of protein-coding genes and lncRNAs in adult Ae. albopictus, which will guide further studies aimed at understanding sex development and determination mechanisms in this species.

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Feminizer and doublesex knock-outs cause honey bees to switch sexes

Cited by 21 publications

References 18 publications

Methylation and gene expression differences between reproductive and sterile bumblebee workers

Methylation and gene expression differences between reproductive and sterile bumblebee workers

Honey bee queens are vulnerable to heat-induced loss of fertility

Differentiation of Long Non-Coding RNA and mRNA Expression Profiles in Male and Female Aedes albopictus

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