A comparison of honeybee (<i>Apis mellifera</i>) queen, worker and drone larvae by RNA‐Seq

He, Xingjian; Jiang, Wu; Zhou, Mi; Barron, Andrew B.

doi:10.1111/1744-7917.12557

Cited by 22 publications

(55 citation statements)

References 39 publications

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“…We asked whether mechanisms identified for maintaining reproductive division of labor in adults also play a role at that stage. While a previous study looking at gene expression during larval caste specification found no differential expression of Dsx (35) , in our experimental perturbation, we found that the gene-level signal was relatively weak ( Figure 1A), possibly due to tissue-specific expression of Dsx (36) , but the network-level signal and its effects were dramatic ( Figure 3A). Therefore we asked whether the Dsx -sensitive module present in adults might also play a similar role in the context of larval caste determination.…”

Section: Does Dsx Play a Role During Larval Caste Differentiation?contrasting

confidence: 73%

“…First, we used an integrated statistic (Z summary ) in the WGCNA package (31) , which tests for preservation of a given module in expression data. According to this test, the Dsx-responsive module detected in our experiment was strongly preserved in whole-body larval gene expression data (35) , meaning that it was also co-expressed in 2 and 4 day old queen-and worker-destined larvae (p = 9.9×10 -7 ). In 4-day old larvae, which have committed to their caste-specific developmental trajectories, these genes were generally upregulated in future queens (rho = 0.083, p = 0.015).…”

Section: Does Dsx Play a Role During Larval Caste Differentiation?mentioning

confidence: 64%

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The Doublesex sex determination pathway regulates reproductive division of labor in honey bees

Velasque

Qiu

Mikheyev

2018

Preprint

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Eusociality, the ultimate level of social organization, requires reproductive division of labor, and a sophisticated system of communication to maintain societal homeostasis. Reproductive division of labor is maintained by physiological differences between reproductive and sterile castes, typically dictated by pheromonal queen fertility signals that suppress worker reproduction. Intriguingly, reproduction and pheromonal signalling share regulatory machinery across insects.The gene Doublesex ( Dsx ) controls somatic sex determination and differentiation, including the development of ovaries and secondary sexual characteristics, such as pheromonal signalling. We hypothesized that this regulatory network was co-opted during eusocial evolution to regulate reproductive division of labor. Taking advantage of the breakdown in reproductive division of labor that occurs in honey bees when workers commence to lay eggs in the absence of a queen, we knocked down Dsx to observe effects on ovary development and fertility signal production. As expected, treated workers had lower levels of egg yolk protein, for which Dsx is a cis-regulatory enhancer in other insects, and greatly reduced ovary development. Also as expected, while control workers increased their levels of pheromonal fertility signals, treated workers did not, confirming the role of Dsx in regulating pheromone biosynthesis. We further found that Dsx is part of a large network enriched for regulatory proteins, which is also involved during early larval development, and upregulated in queen-destined larvae. Thus, the ancient developmental framework controlling sex specification and reproduction in solitary insects has been exapted for eusociality, forming the basis for reproductive division of labor and pheromonal signalling pathways. Significance statementComplex social insect societies rely on division of reproductive labor among their members. Reproductive individuals ('queens') suppress 'worker' reproduction using pheromonal fertility signalling. We show that an ancient regulatory network that controls specification of sex and secondary sexual characteristics in solitary insects, has been co-opted for both both pheromonal signalling and ovary inactivation in honey bees. In addition, this network is also active during caste specification that takes place during the first few days of larval life. These results show that pheromonal signalling and ovary development share a common regulatory framework, potentially explaining why fertility signalling is 'honest.' Furthermore, they show that higher levels of biological complexity can arise by rewiring and elaborating ancestral gene regulatory networks.

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Section: Does Dsx Play a Role During Larval Caste Differentiation?contrasting

confidence: 73%

Section: Does Dsx Play a Role During Larval Caste Differentiation?mentioning

confidence: 64%

The Doublesex sex determination pathway regulates reproductive division of labor in honey bees

Velasque

Qiu

Mikheyev

2018

Preprint

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“…We found no significant under or over enrichment in the 100 slowest evolving NCARs. Of the 15,314 genes in the A. mellifera OGS v3.2, 209 were found to be queen-biased and 276 were found to be worker-biased in four day old larvae [22]. Only 16 and 31 NCARs were proximal to queen-and worker-biased genes, respectively.…”

Section: Expression Bias In Foragers and Nursesmentioning

confidence: 95%

Rate variation in the evolution of non-coding DNA associated with social evolution in bees

Jones

Hunt

et al. 2019

Phil. Trans. R. Soc. B

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The evolutionary origins of eusociality represent increases in complexity from individual to caste-based, group reproduction. These behavioural transitions have been hypothesized to go hand in hand with an increased ability to regulate when and where genes are expressed. Bees have convergently evolved eusociality up to five times, providing a framework to test this hypothesis. To examine potential links between putative gene regulatory elements and social evolution, we compare alignable, non-coding sequences in 11 diverse bee species, encompassing three independent origins of reproductive division of labour and two elaborations of eusocial complexity. We find that rates of evolution in a number of non-coding sequences correlate with key social transitions in bees. Interestingly, while we find little evidence for convergent rate changes associated with independent origins of social behaviour, a number of molecular pathways exhibit convergent rate changes in conjunction with subsequent elaborations of social organization. We also present evidence that many novel non-coding regions may have been recruited alongside the origin of sociality in corbiculate bees; these loci could represent gene regulatory elements associated with division of labour within this group. Thus, our findings are consistent with the hypothesis that gene regulatory innovations are associated with the evolution of eusociality and illustrate how a thorough examination of both coding and non-coding sequence can provide a more complete understanding of the molecular mechanisms underlying behavioural evolution. This article is part of the theme issue ‘Convergent evolution in the genomics era: new insights and directions’.

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“…To investigate the relationship between conserved non-coding regions and genes with castebiased expression in Apis mellifera, we examined genes that are expressed at different levels in virgin queens versus sterile workers for both adults [50] and larvae [51] as well as those differentially expressed between nurses and foragers, which represent categories of age-based worker polyethism [52]. Of the 3,610 genes compared between workers and queen adults, 587 are worker-biased and 649 are queen-biased.…”

Section: Associations Between Ncars and Caste-biased Gene Expressionmentioning

confidence: 99%

“…Finally, within the honey bees, most large studies compare differences between adult bees [50,52], while the NCARs we have identified could affect gene expression at any point throughout development, and it is impossible to predict when, where, and in what context gene expression changes may occur. Although we did examine overlap with genes differentially expressed between worker and queen larvae (Supplementary Information), these results were based on a relatively small dataset and may have only captured those genes with the most extreme expression differences [51].…”

Section: A Subset Of Ncars Are Associated With Gene Expression Differmentioning

confidence: 99%

Rate variation in the evolution of non-coding DNA associated with social evolution in bees

Jones

Hunt

et al. 2018

Preprint

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14The evolutionary origins of eusociality represent increases in complexity from individual to caste-15 based, group reproduction. These behavioral transitions have been hypothesized to go hand-in- 16hand with an increased ability to regulate when and where genes are expressed. Bees have 17 convergently evolved eusociality up to five times, providing a framework to test this hypothesis. 18To examine potential links between putative gene regulatory elements and social evolution, we 19 compare alignable, non-coding sequences in eleven diverse bee species, encompassing three 20 independent origins of reproductive division of labor and two elaborations of eusocial complexity. 21We find that rates of evolution in a number of non-coding sequences correlate with key social 22 transitions in bees. Interestingly, while we find little evidence for convergent rate changes 23 associated with independent origins of social behavior, a number of molecular pathways exhibit 24 convergent rate changes in conjunction with subsequent elaborations of social organization. We 25 also present evidence that many novel non-coding regions may have been recruited alongside 26 the origin of sociality in corbiculate bees; these loci could represent gene regulatory elements 27 associated with division of labor within this group. Thus, our findings are consistent with the 28 hypothesis that gene regulatory innovations are associated with the evolution of eusociality and 29 illustrate how a thorough examination of both coding and non-coding sequence can provide a 30 more complete understanding of the molecular mechanisms underlying behavioral evolution. 32 33Introduction 34 35Many genomic sequences that do not encode proteins play essential roles in gene regulation 36 across animals [1] and plants [2]. The breadth of knowledge of these non-coding regulatory 37 elements has been built primarily upon the large number of plant and vertebrate genomes that 38 have been sequenced over the past decade. However, the high degree of conservation that exists 39 in a subset of these non-coding regions [1,3] means that comparative methods can be used to 40 identify similar non-coding elements even in the recently sequenced genomes of non-model taxa 41 that frequently lack the resources needed to characterize regulatory regions via functional assays. outside of Drosophila [4], the non-coding regulatory landscape of these taxa has been the target 44 of few studies. 46Here, we take advantage of eleven publicly-available bee genomes [5][6][7][8][9] to examine how non-47 coding elements change as eusociality -an extreme form of social behavior found primarily in 48 insects and mammals -has convergently evolved and increased in complexity within bees. 49Eusociality is of particular interest to evolutionary biologists because it represents an increase in 50 complexity from individual to group-level reproduction and includes the evolution of a non-51 reproductive worker caste [10]. Along with reproductively-specialized castes, many of these 52 societies have also e...

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A comparison of honeybee (Apis mellifera) queen, worker and drone larvae by RNA‐Seq

Cited by 22 publications

References 39 publications

The Doublesex sex determination pathway regulates reproductive division of labor in honey bees

The Doublesex sex determination pathway regulates reproductive division of labor in honey bees

Rate variation in the evolution of non-coding DNA associated with social evolution in bees

Rate variation in the evolution of non-coding DNA associated with social evolution in bees

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