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Age at which larvae are orphaned determines their development into typical or rebel workers in the honeybee (Apis mellifera L.).

Kuszewska K, Woyciechowski M - PLoS ONE (2015)

Bottom Line: These rebel workers are more queenlike and have greater reproductive potential than normal workers.However, it was unclear whether larvae orphaned at any time during their feeding period can develop into rebels.Our results showed that larvae orphaned during the final four or more days of their feeding life develop into rebel workers with more ovarioles in their ovaries, smaller hypopharyngeal glands, and larger mandibular and Dufour's glands compared with typical workers with low reproductive potential that were reared with a queen or orphaned at the third to last or a later day of feeding life.

View Article: PubMed Central - PubMed

Affiliation: Institute of Environmental Sciences, Jagiellonian University, Krakow, Poland.

ABSTRACT
In the honeybee, diploid larvae fed with royal jelly develop into reproductive queens, whereas larvae fed with royal jelly for three days only and subsequently with honey and pollen develop into facultatively sterile workers. A recent study showed that worker larvae fed in a queenless colony develop into another female polyphenic form: rebel workers. These rebel workers are more queenlike and have greater reproductive potential than normal workers. However, it was unclear whether larvae orphaned at any time during their feeding period can develop into rebels. To answer this question, the anatomical features of newly emerged workers reared in queenless conditions at different ages during the larval period were evaluated. Our results showed that larvae orphaned during the final four or more days of their feeding life develop into rebel workers with more ovarioles in their ovaries, smaller hypopharyngeal glands, and larger mandibular and Dufour's glands compared with typical workers with low reproductive potential that were reared with a queen or orphaned at the third to last or a later day of feeding life.

No MeSH data available.


Related in: MedlinePlus

Time schedule of manipulations and the experimental days when workers were sampled from the seven groups (indicated in green).The time of egg incubation is indicated in blue; feeding larvae (unsealed larvae) are indicated in red; and sealed larvae or pupae are indicated in black.
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pone.0123404.g001: Time schedule of manipulations and the experimental days when workers were sampled from the seven groups (indicated in green).The time of egg incubation is indicated in blue; feeding larvae (unsealed larvae) are indicated in red; and sealed larvae or pupae are indicated in black.

Mentions: The research was conducted in July 2010 in the experimental apiary of the Institute of Environmental Sciences (Jagiellonian University, Krakow, southern Poland). Five queenright honeybee (A. m. carnica) colonies were studied, each consisting of 20 000–40 000 workers. All colonies were treated in the same way, as shown in Fig 1. Before the experiment began, three empty frames of wax combs were placed in each experimental colony to increase the area available for eggs laying by the queen. At the beginning of the experiment, each colony was temporarily orphaned (day 0), and each queen was transferred to a new hive box with a small group of workers. Workers, pupae, sealed larvae and unsealed larvae of different ages remained in the native queenless colonies. One week after orphaning (day 7), the queens were transferred back to their native colonies. As a result of this manipulation, larvae were reared under seven different conditions (groups 0–6; Fig 1) inside each native colony. The larvae of group 0 were raised in the queenright condition during their entire feeding period, before the colony was orphaned. The larvae from groups 1 to 5 were raised in the queenless condition for the last 1 to 5 days of their feeding period, respectively. Larvae of group 6 hatched from eggs after the queen was transferred to the new hive box, such that they were reared in the queenless condition during their whole feeding period. On day 12 of the experiment, the frames with sealed broods were transferred from each colony to the laboratory, and 30 newly emerged workers (reared as larvae in the queenright condition—group 0) were sampled. This procedure was repeated for 7 consecutive days (from day 12 to 18 of the experiment; Fig 1) to sample the workers reared as larvae without the queen for different numbers of days (groups 0–6; all workers from all experimental groups emerged in an incubator in the laboratory). All of these workers were weighed and killed by freezing (–16°C) and subsequently dissected under a stereomicroscope (binocular loupe). The number of ovarioles and the sizes of the hypopharyngeal, mandibular and Dufour’s glands were determined to discriminate rebel and non-rebel works [23]. In honeybees, the number of ovarioles is a good indicator of the reproductive potential of females [27,28], and the mandibular and Dufour’s glands are usually larger in queens and reproductive workers than in non-reproductive workers [11]. The size of the hypopharyngeal glands, which synthesize and store brood food, depends on the social status of workers [29,30] and are largest in nursing bees [31]. The total number of ovarioles in both ovaries of each worker was recorded. The size of the hypopharyngeal glands was calculated from the average of 10 acini (each acinus was measure as the square root of the longest × shortest diameter, and the average was calculated from 5 acini from the right gland and 5 from the left gland). The hypopharyngeal gland consists of a great number of lobes, called acini, and their diameter is routinely used as an index of gland size [23,32–34]. The size of the mandibular gland was calculated from the average of the left and right glands (each gland was measure as the square root of the longest × shortest diameter). The size of Dufour’s gland was also calculated as the square root of the longest × shortest diameters. All organs were stained with Giemsa reagent (approximately 10 seconds) before measured.


Age at which larvae are orphaned determines their development into typical or rebel workers in the honeybee (Apis mellifera L.).

Kuszewska K, Woyciechowski M - PLoS ONE (2015)

Time schedule of manipulations and the experimental days when workers were sampled from the seven groups (indicated in green).The time of egg incubation is indicated in blue; feeding larvae (unsealed larvae) are indicated in red; and sealed larvae or pupae are indicated in black.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4400021&req=5

pone.0123404.g001: Time schedule of manipulations and the experimental days when workers were sampled from the seven groups (indicated in green).The time of egg incubation is indicated in blue; feeding larvae (unsealed larvae) are indicated in red; and sealed larvae or pupae are indicated in black.
Mentions: The research was conducted in July 2010 in the experimental apiary of the Institute of Environmental Sciences (Jagiellonian University, Krakow, southern Poland). Five queenright honeybee (A. m. carnica) colonies were studied, each consisting of 20 000–40 000 workers. All colonies were treated in the same way, as shown in Fig 1. Before the experiment began, three empty frames of wax combs were placed in each experimental colony to increase the area available for eggs laying by the queen. At the beginning of the experiment, each colony was temporarily orphaned (day 0), and each queen was transferred to a new hive box with a small group of workers. Workers, pupae, sealed larvae and unsealed larvae of different ages remained in the native queenless colonies. One week after orphaning (day 7), the queens were transferred back to their native colonies. As a result of this manipulation, larvae were reared under seven different conditions (groups 0–6; Fig 1) inside each native colony. The larvae of group 0 were raised in the queenright condition during their entire feeding period, before the colony was orphaned. The larvae from groups 1 to 5 were raised in the queenless condition for the last 1 to 5 days of their feeding period, respectively. Larvae of group 6 hatched from eggs after the queen was transferred to the new hive box, such that they were reared in the queenless condition during their whole feeding period. On day 12 of the experiment, the frames with sealed broods were transferred from each colony to the laboratory, and 30 newly emerged workers (reared as larvae in the queenright condition—group 0) were sampled. This procedure was repeated for 7 consecutive days (from day 12 to 18 of the experiment; Fig 1) to sample the workers reared as larvae without the queen for different numbers of days (groups 0–6; all workers from all experimental groups emerged in an incubator in the laboratory). All of these workers were weighed and killed by freezing (–16°C) and subsequently dissected under a stereomicroscope (binocular loupe). The number of ovarioles and the sizes of the hypopharyngeal, mandibular and Dufour’s glands were determined to discriminate rebel and non-rebel works [23]. In honeybees, the number of ovarioles is a good indicator of the reproductive potential of females [27,28], and the mandibular and Dufour’s glands are usually larger in queens and reproductive workers than in non-reproductive workers [11]. The size of the hypopharyngeal glands, which synthesize and store brood food, depends on the social status of workers [29,30] and are largest in nursing bees [31]. The total number of ovarioles in both ovaries of each worker was recorded. The size of the hypopharyngeal glands was calculated from the average of 10 acini (each acinus was measure as the square root of the longest × shortest diameter, and the average was calculated from 5 acini from the right gland and 5 from the left gland). The hypopharyngeal gland consists of a great number of lobes, called acini, and their diameter is routinely used as an index of gland size [23,32–34]. The size of the mandibular gland was calculated from the average of the left and right glands (each gland was measure as the square root of the longest × shortest diameter). The size of Dufour’s gland was also calculated as the square root of the longest × shortest diameters. All organs were stained with Giemsa reagent (approximately 10 seconds) before measured.

Bottom Line: These rebel workers are more queenlike and have greater reproductive potential than normal workers.However, it was unclear whether larvae orphaned at any time during their feeding period can develop into rebels.Our results showed that larvae orphaned during the final four or more days of their feeding life develop into rebel workers with more ovarioles in their ovaries, smaller hypopharyngeal glands, and larger mandibular and Dufour's glands compared with typical workers with low reproductive potential that were reared with a queen or orphaned at the third to last or a later day of feeding life.

View Article: PubMed Central - PubMed

Affiliation: Institute of Environmental Sciences, Jagiellonian University, Krakow, Poland.

ABSTRACT
In the honeybee, diploid larvae fed with royal jelly develop into reproductive queens, whereas larvae fed with royal jelly for three days only and subsequently with honey and pollen develop into facultatively sterile workers. A recent study showed that worker larvae fed in a queenless colony develop into another female polyphenic form: rebel workers. These rebel workers are more queenlike and have greater reproductive potential than normal workers. However, it was unclear whether larvae orphaned at any time during their feeding period can develop into rebels. To answer this question, the anatomical features of newly emerged workers reared in queenless conditions at different ages during the larval period were evaluated. Our results showed that larvae orphaned during the final four or more days of their feeding life develop into rebel workers with more ovarioles in their ovaries, smaller hypopharyngeal glands, and larger mandibular and Dufour's glands compared with typical workers with low reproductive potential that were reared with a queen or orphaned at the third to last or a later day of feeding life.

No MeSH data available.


Related in: MedlinePlus