Down-Regulation of Honey Bee IRS Gene Biases Behavior toward Food Rich in Protein

Wang, Ying; Mutti, Navdeep S.; Ihle, Kate E.; Siegel, Adam J.; Doležal, Adam; Kaftanoğlu, Osman; Amdam, Gro V.

doi:10.1371/journal.pgen.1000896

Cited by 88 publications

(82 citation statements)

References 76 publications

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“…Worker honey bees undergo an agerelated division of labor that allows them to transition from inhive tasks to foraging and colony defense over time. This division of labor is regulated through an unusual interaction between the egg yolk protein Vitellogenin (Vg), juvenile hormone (JH) and JH-signaling, and insulin-like/TOR signaling (40)(41)(42)(43)(44)(45)(46) (Fig. 3B).…”

Section: Resultsmentioning

confidence: 99%

Population genomics of the honey bee reveals strong signatures of positive selection on worker traits

Harpur¹,

Kent²,

Molodtsova³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

194

271

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Most theories used to explain the evolution of eusociality rest upon two key assumptions: mutations affecting the phenotype of sterile workers evolve by positive selection if the resulting traits benefit fertile kin, and that worker traits provide the primary mechanism allowing social insects to adapt to their environment. Despite the common view that positive selection drives phenotypic evolution of workers, we know very little about the prevalence of positive selection acting on the genomes of eusocial insects. We mapped the footprints of positive selection in Apis mellifera through analysis of 40 individual genomes, allowing us to identify thousands of genes and regulatory sequences with signatures of adaptive evolution over multiple timescales. We found Apoidea-and Apis-specific genes to be enriched for signatures of positive selection, indicating that novel genes play a disproportionately large role in adaptive evolution of eusocial insects. Worker-biased proteins have higher signatures of adaptive evolution relative to queen-biased proteins, supporting the view that worker traits are key to adaptation. We also found genes regulating worker division of labor to be enriched for signs of positive selection. Finally, genes associated with worker behavior based on analysis of brain gene expression were highly enriched for adaptive protein and cis-regulatory evolution. Our study highlights the significant contribution of worker phenotypes to adaptive evolution in social insects, and provides a wealth of knowledge on the loci that influence fitness in honey bees.natural selection | kin selection | social evolution | taxonomically restricted genes E usocial behavior evolved multiple times in insects and is characterized in part by extreme asymmetries in the reproductive potential of individuals (1). This asymmetry is most pronounced in advanced eusocial insects, with their fertile queen and sterile worker castes. Darwin first recognized that natural selection cannot directly optimize worker phenotypes because workers are usually sterile (2). Hamilton (3, 4) developed kinselection theory to describe the conditions that allow natural selection to indirectly optimize worker phenotypes if such phenotypes benefit their fertile kin. It is commonly believed that worker traits, such as sib-care, foraging, and colony defense, play important roles in allowing colonies to adapt to their environment (5-7). However, despite the central role of kin-selection and inclusive fitness theory in the field of Sociobiology (8, 9), we lack knowledge on the pattern and prevalence of positive selection acting on the genomes of eusocial insects.Population genomic studies provide unprecedented opportunities to detect signatures of selection on DNA sequences over different timescales (10). There are several tests of selection that can be applied to genome-wide datasets. The McDonald-Kreitman (MK) test is arguably the best method for detecting selection on protein coding sequences because of its robustness to changes in a species' demography,...

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Section: Resultsmentioning

confidence: 99%

Population genomics of the honey bee reveals strong signatures of positive selection on worker traits

Harpur¹,

Kent²,

Molodtsova³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

194

271

View full text Add to dashboard Cite

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“…Under shortages of pollen or in conditions of poor pollen quality, honey bee colonies increase the proportion of pollen foragers without increasing foraging rate (Pernal and Currie 2010). The foraging choice between pollen (protein) and nectar (carbohydrate sources) is influenced by insulin receptor substrate (IRS) as demonstrated by Wang et al (2010). It seems that the foraging tasks are under the control of many factors and detailed studies on these factors are required.…”

Section: Foraging Tasksmentioning

confidence: 99%

The foraging behaviour of honey bees, Apis mellifera: a review

Abou‐Shaara¹

2014

Vet. Med.

177

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Foraging behaviour is one of the distinctive behaviours of honey bees, Apis mellifera. This behaviour is the link between the honey bee colony and the ambient environment. Therefore, various in-colony and out-colony factors have an impact on this behaviour, and many studies have been employed to investigate these factors. Foraging behaviour is not advantageous only for the colony and for plant pollination but also has other benefits. In contrast, some disadvantages have also been discovered to be linked with foraging activity. Practically speaking, the control over this behaviour is very important to maximize colony products as well as to increase other agricultural benefits. This paper presents a review on foraging activity including; the regulation of foraging tasks, factors impacting this behaviour, foraging preference, variations between subspecies, monitoring methods as well as the possible methods for controlling this behaviour. As concluded from this review, more work needs to be performed in order to elucidate certain aspects of foraging behaviour.

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“…Bees were mounted in holders (see Hammer and Menzel, 1995) before gustatory responsiveness was quantified, as detailed previously (Wang et al, 2010). In brief, operators were blind to the treatment identity of the bees.…”

Section: Measurements Of Gustatory Responsivenessmentioning

confidence: 99%

Flight restriction prevents associative learning deficits but not changes in brain protein-adduct formation during honeybee ageing

Tolfsen

Baker

Kreibich

et al. 2011

Journal of Experimental Biology

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SUMMARYHoneybees (Apis mellifera) senesce within 2weeks after they discontinue nest tasks in favour of foraging. Foraging involves metabolically demanding flight, which in houseflies (Musca domestica) and fruit flies (Drosophila melanogaster) is associated with markers of ageing such as increased mortality and accumulation of oxidative damage. The role of flight in honeybee ageing is incompletely understood. We assessed relationships between honeybee flight activity and ageing by simulating rain that confined foragers to their colonies most of the day. After 15days on average, flight-restricted foragers were compared with bees with normal (free) flight: one group that foraged for ~15days and two additional control groups, for flight duration and chronological age, that foraged for ~5days. Free flight over 15days on average resulted in impaired associative learning ability. In contrast, flight-restricted foragers did as well in learning as bees that foraged for 5days on average. This negative effect of flight activity was not influenced by chronological age or gustatory responsiveness, a measure of the bees' motivation to learn. Contrasting their intact learning ability, flight-restricted bees accrued the most oxidative brain damage as indicated by malondialdehyde protein adduct levels in crude cytosolic fractions. Concentrations of mono-and poly-ubiquitinated brain proteins were equal between the groups, whereas differences in total protein amounts suggested changes in brain protein metabolism connected to forager age, but not flight. We propose that intense flight is causal to brain deficits in aged bees, and that oxidative protein damage is unlikely to be the underlying mechanism.Supplementary material available online at

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Down-Regulation of Honey Bee IRS Gene Biases Behavior toward Food Rich in Protein

Cited by 88 publications

References 76 publications

Population genomics of the honey bee reveals strong signatures of positive selection on worker traits

Population genomics of the honey bee reveals strong signatures of positive selection on worker traits

The foraging behaviour of honey bees, Apis mellifera: a review

Flight restriction prevents associative learning deficits but not changes in brain protein-adduct formation during honeybee ageing

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