Complex patterns of differential expression in candidate master regulatory genes for social behavior in honey bees

Johnson, Brian R.; Jasper, W. Cameron

doi:10.1007/s00265-016-2071-9

Cited by 28 publications

(34 citation statements)

References 94 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: 75%

“…Aggregating data at the whole body or body part level is common practice in social insect gene expression studies, but this likely increases the signal-to-noise ratio. This hypothesis is supported by the observation that the only study to date that has detected significant differences in Dsx in honey bees analyzed tissue-specific expression (36) . Furthermore, because Dsx interacts with many other genes, its levels may be constrained within fairly narrow ranges, making differences harder to detect.…”

Section: Discussionmentioning

confidence: 73%

“…If Dsx is central to reproductive division of labor in honey bees, why has it not been picked up by other studies as a core gene involved in caste determination, even those that specifically tested for its differential expression (e.g., (35) )? Expression of Dsx is highly tissue-specific (36,41,56) . Aggregating data at the whole body or body part level is common practice in social insect gene expression studies, but this likely increases the signal-to-noise ratio.…”

Section: Discussionmentioning

confidence: 99%

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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: 75%

Section: Discussionmentioning

confidence: 73%

Section: Discussionmentioning

confidence: 99%

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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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“…In this paper, we provide several examples from molecular analyses of the honeybee worker sterility to illustrate how accessible -omics data sets can be effectively assembled into networks, representing a robust way to gain new insights into the molecular regulation of social traits. First, we join others to argue that a systems level network approach can serve as an adjunct to the field of sociogenomic biology (Chandrasekaran et al, 2011;Charbonneau et al, 2013;Fewell, 2003;Foster, 2011;Johnson & Jasper, 2016;Kapheim, 2016;Linksvayer et al, 2012;Morandin et al, 2016;Sobotka et al, 2016). Converting lists of coexpressed genes into graphical networks can help identify and prioritize genes based on their positioning within the network.…”

Section: Discussionmentioning

confidence: 98%

“…Other network studies from social insects reveal that a gene's position and rank within its regulatory context can influence its capacity for cis ‐regulation via methylation (Foret, Kucharski, Pittelkow, Lockett, & Maleszka, ), its propensity to direct and coordinate aspects of caste differentiation (Abouheif & Wray, ; Barchuk et al, ; Johnson & Jasper, ) and its ability to regulate the worker's retinue response to queen pheromone (Kocher et al, ). Likewise, specific network gene clusters have been implicated in worker temperament (Alaux et al, ), worker ovary activation (Thompson et al, ), nurse‐to‐forager maturation (Ament et al, ), and other behavioral traits that characterize social reproduction (Amdam, Page, Fondrk, & Brent, ; Ament, Corona, Pollock, & Robinson, ; Hunt et al, ; Wang et al, ).…”

Section: Idea To Practice: Gene Network In Sociobiologymentioning

confidence: 99%

From gene list to gene network: Recognizing functional connections that regulate behavioral traits

et al. 2018

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The study of social breeding systems is often gene focused, and the field of insect sociobiology has been successful at assimilating tools and techniques from molecular biology. One common output from sociogenomic studies is a gene list. Gene lists are readily generated from microarray, RNA sequencing, or other molecular screens that typically aim to prioritize genes based on the differences in their expression. Gene lists, however, are often unsatisfying because the information they provide is simply tabular and does not explain how genes interact with each other, or how genetic interactions change in real time under social or environmental circumstances. Here, we promote a view that is relatively common to molecular systems biology, where gene lists are converted into gene networks that better describe the functional connections that regulate behavioral traits. We present a narrative related to honeybee worker sterility to show how network analysis can be used to reprioritize candidate genes based on connectivity rather than their freestanding expression values. Networks can also reveal multigene modules, motifs, clusters or other system‐wide properties that might not be apparent from an ab initio list. We argue that because network analyses are not restricted to “genes” as nodes, their implementation can potentially connect multiple levels of biological organization into a single, progressively complex study system.

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Sexual dimorphism as a facilitator of worker caste evolution in ants

Smith

2023

Ecology and Evolution

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Ant societies are primarily composed of females, whereby labor is divided into reproductive, or queen, and non‐reproductive, or worker, castes. Workers and reproductive queens can differ greatly in behavior, longevity, physiology, and morphology, but queen–worker differences are usually modest relative to the differences in males. Males are short‐lived, typically do not provide the colony with labor, often look like a different species, and only occur seasonally. It is these differences that have historically led to their neglect in social insect research, but also why they may facilitate novel phenotypic variation – by increasing the phenotypic variability that is available for selection. In this study, worker variation in multivariate size–shape space paralleled male–queen variation. As worker variation increased within species, so did sexual variation. Across species in two independent genera, using head width as a proxy for body size, sexual size dimorphism correlated with worker polymorphism regardless of whether the ancestral condition was large or small worker/sexual dimorphism. Mounting molecular data support the hypothesis that queen–worker caste determination has co‐opted many genes/pathways from sex determination. The molecular evidence, coupled with the observations from this study, leads to the hypothesis that sexual selection and selection on colony‐level traits are non‐independent, and that sexual dimorphism may even have facilitated the evolution of the distinct worker caste.

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Complex patterns of differential expression in candidate master regulatory genes for social behavior in honey bees

Cited by 28 publications

References 94 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

From gene list to gene network: Recognizing functional connections that regulate behavioral traits

Sexual dimorphism as a facilitator of worker caste evolution in ants

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