The Individual
Francis L. W. Ratnieks
Social Insects: C1139
Laboratory of Apiculture
& Social Insects
Department of Biological
& Environmental Science
University of Sussex
Aims & Objectives
Present roles & specializations of individuals with main
emphasis on bees, wasps, ants (Hymenoptera)
Females
Males
Non-adults (brood)
Primary division of labour: reproducing v working
queens (reproduction) & workers (work)
Stages in the loss of worker reproductive ability
Big Picture
The individual is the building block of the society
A colony is a functional adaptive unit
(Although there may also be conflict among the individuals)
Like cells in a body there are different types of individuals
The types and their roles vary among different taxa
Unlike cells in a multi-cellular organism they are unfused
(Unlike cells in a multi-cellular organism , relatedness < 1)
Big Picture: Reproductive Division of Labour
Reproductive division of labour
The key defining feature of eusociality
Colonies have reproductive individuals
Female: Queen
Male: King in termites, sperm in Hymenoptera
Often but not always just one queen per colony
Colonies have non-reproductive individuals: Workers
But workers sometimes reproduce & queens sometimes work
Brood
A. mellifera Comb With Brood & Nectar
A. mellifera Egg in Base of Cell
A. mellifera Pupae in Wax-Capped Cells
Brood
Vespinae Wasp Brood
The brood of Vespinae and
Polistinae wasps are held in
hexagonal cells. The larvae are fed
gradually (“Progressive
provisioning”) and then pupate.
The larva spins a cocoon which
seals the cell.
Photos
Top row left: eggs
Bottom row: pupae
Others: larvae
Wasp Larvae Help Colony Nutrition
Common Wasp Vespula vulgaris
In Vespinae wasps, the larvae have
very large salivary glands. They
feed larvae insect prey. The larvae
convert protein into sugars. Adults
consume a nutritious saliva
secreted by the larvae.
In Japan, you can buy a sports
drink called VAAM (Vespa Amino
Acid Mixture) based on the saliva
of hornets, Vespa. The Japanese
woman who won the marathon in
the Sydney Olympics was drinking
it as she ran.
Hornet Saliva Powers Sydney Marathon Gold
As it says above, the Japanese woman who won the marathon at the
Sydney Olympics was drinking VAAM: Vespa amino acid mixture.
Oecophylla Weaver Ants: Larval Silk
The two species of
Oecophylla
weaver ant are
found in Africa,
Asia, and
Australia. They
have massive
colonies and nest
in trees. The nest
is woven from live
tree leaves held
together with
larval silk. The
larva is used like a
living glue gun by
the workers. The
workers also form
living chains to
pull leaves
together before
gluing in position.
Camponotus senex, New Nest
Camponous senex colony building a new nest. Like weaver ants they use
larva as glue guns. Unlike weaver ants they do not pull the leaves
together before gluing them. Photos Sao Paulo, Brazil.
Role of Brood in Eusocial Hymenoptera
Hymenoptera are holometabolous with egg, larva, pupa and
adult stages. Queens and workers are adults. The larvae are
passive, lacking legs and normally just immobile in a cell
(most bees & wasps) or in a brood pile (ants). They are fed by
the workers. In most species they don’t do anything other than
grow.
In a few taxa they perform some function for the colony. The
use of larval silk in nest building has evolved three times in
ants. In Vespidae wasps the larvae help digest protein food,
which they can convert into sugars and feed back to the
workers and queen in their saliva.
Larvae can also be cannibalized if there is a food shortage.
Termite Nymphs: Soldier & Worker
These individuals of the primitive termite, Zootermopsis nevadensis from
California, including the soldier on the left, are nymphs and can
potentially metamorphose into reproductives.
Role of Brood in Termites, Isoptera
Isoptera are hemimetabolous with egg, nymph and adult
stages. Queens and males are true adults, usually with wings.
The workers and soldiers are nymphs. In termites, work is
based on child labour.
In the higher termites (Termitidae, which include the species
that build huge nests in Africa and cultivate fungus) the
workers are a terminal caste of sterile nymphs. That is, they
cannot metamorphose into another stage, such as into a
reproductive individual.
In most termites working individuals can metamorphose into
reproductive individuals.
Males
Eusocial Hymenopteran Males
The forgotten sex in eusocial Hymenoptera
Most attention is focused on females
workers are always female
no king: father present only as sperm
queen stores lifetime sperm supply from nuptial flight
Males are haploid
arise from unfertilized eggs
eggs laid by workers are generally male
Diploid males can occur
they are a genetic dead end
arise due to limitations in the sex-determination process
Eusocial Hymenopteran Males
One or two generations of males present in a colony
Parental Generation
Sperm stored in the queen’s spermatheca
Disembodied father
Offspring Generation
Males being reared as reproductives
Brood and adults
Only part of the year
Can be queen’s sons and workers’ sons
Eusocial Hymenopteran Males
Eusocial hymenopteran male is normally
Winged
Mates away from the nest
Does not work
Does not influence colony reproduction
Never co-founds nest with the queen
However, males can show specialisations that are a
consequence of eusociality.
Drone & Worker Honey Bees
Two drones and workers on a comb. The drone is designed via sexual
selection for male-male competition, with large eyes and flight muscles,
to out-compete other males when chasing queens on mating flights.
Many males chase each queen leading to strong scramble competition.
Honey Bee Swarm
Small swarm of Apis mellifera, c. 5000 bees, in a bush.
Honey Bee Swarm, Close Up
Very few drones leave the parent colony with the swarm
Mating
Common Wasps
Mating common wasps, Vespula vulgaris. Male is above
Male Bumble Bee
Male bumble bees and common wasps feed themselves at
flowers. They can be recognized by their long antennae
Mating Dinosaur Ants
Above. Mating dinosaur ants,
Dinoponera quadriceps. The
male is winged and red in
colour. He is mating to a
worker. In this species of ant
the morphological queen caste
has been lost and the colony is
headed by a mated worker
(sometime called a
“gamergate”) who is the
functional queen. This is
unusual.
Below. The male is unwilling
to disengage so the female
severs his genitalia.
Honey Bee Mating Plug
Queen honey bee caught as she
returns to her hive. The white
material in the tip of her
abdomen is the genitalia of the
last male she mated with. In
the honey bee Apis mellifera
the male can only mate once.
His genitalia cannot be
retracted and break off during
mating, where they function as
a mating plug preventing the
semen leaking out of the
queen.
However, the mating plug does
not prevent other males from
mating the queen as they can
easily remove it.
Male Work
In some stingless bees males may secrete wax and in bumble
bees males may help incubate brood.
Why don’t hymenopteran males work?
The reason is almost certainly not to do with relatedness.
Rather it is because in subsocial Hymenoptera it is only the
female who builds the nest and provisions and looks after the
young. Thus, only the females were preadapted to helping.
Non-domesticated males originated in subsocial Hymenoptera
and carried over to eusocial Hymenoptera.
Male Reproductive Interests
Because males are not involved in brood rearing, they can
have little influence on colony reproduction, for example
causing the colony to rear the ratio of queens and males (sex
allocation) that is optimal for their interests.
However, there are a few cases where certain male
reproductive interests can be fulfilled. In the honey bee Apis
mellifera, very few males join the swarm. It is better for
everyone if they remain in the parental nest where food is
abundant.
In Cardiocondyla ants there are worker-like males without
wings and with large mandibles. In this species mating can
also occur in the nest. The worker-like males mate in the nest
with young sister queens. They also fight with each other.
They do not kill winged males, who normally mate outside the
nest, as the winged males smell like females.
Effects of Eusociality on Males
In some eusocial insects, the number of males greatly
outnumbers the number of females that need to get mated
because new colonies are formed by colony fission. In the
honey bee this is known as swarming. “Female” reproduction
is a swarm, which is mostly workers with one queen. In
Dinoponera quadriceps ants colonies divide without swarming
and only one female needs to be mated.
In these species most males never mate. Those that do put
everything into the first mating with their genitalia acting as a
mating plug. It is better to slightly increase paternity from a
single mating than to hold back and hope for a second mating.
These examples show that eusociality can have effects on the
reproductive behaviour of males. In addition, males in many
species do not need to forage and can be designed for a single
purpose–mating. In the honey bee intense male-male scramble
competition has led to large fast-flying males.
Females
Queens & Workers Morphologically Distinct
Bombus terrestris
bumble bee
Lasius niger
pavement ant
Apis mellifera
honey bee
Atta cephalotes
leafcutter ant
Vespula vulgaris
common wasp
Dorylus wilverthi
driver or army ant
Queen Honey Bee Laying Egg
Honey Bee: Female Reproductive Systems
queen
worker
ovaries
spermatheca
An Apis mellifera queen has massive ovaries with hundreds of ovarioles,
and can lay up to 2000 eggs per day. She has a large spherical spermstorage organ in which she can keep sperm alive for years. The workers
have smaller ovaries, a vestigial spermatheca, and cannot mate.
Honey Bee Queen Rearing
Apis mellifera queens are reared in special queen cells on special food
known as royal jelly. The special cell triggers the feeding of royal jelly
by workers, and the royal jelly triggers the larva to develop as a queen.
Honey Bee Queen Rearing
Type of Cell
Queen lays
Workers feed
larvae with
Duration from
egg to adult
Unfertilized egg
Normal brood food
24 days
Fertilized egg
Normal brood food
21 days
Fertilized egg
Royal jelly
16 days
Drone cell 20%
of comb area
Worker cell 80%
of comb area
Queen cell 10-30 in
swarming season
Honey Bee Queen Rearing
queen
Female
egg
Female
larva
worker
In the honey bee, and in most eusocial Hymenoptera with
morphologically-distinct queen and worker castes, any female can
develop into either a queen or a worker. In most species the
developmental programs diverge in the larval stage.
Honey Bee Queen Rearing
Royal jelly is rich in mandibular gland secretions of workers. The quality
of food in the first 3 days determines caste fate. Larvae <3 days old are
totipotent. After this they have chosen one pathway or the other.
Commercial queen rearing involves transferring one-day-old larvae from
worker cells into queen cells.
Commercial Queen Rearing
Capped queen cells reared from plastic cells bases. A one-day
old female larva is transferred into a queen cup and placed into
a hive without a queen. The larvae is fed royal jelly and the
cell is extended. The queens have emerged from the two cells
in the centre.
Queen Rearing
In almost all species of eusocial Hymenoptera with
morphologically-distinct queen and worker castes, a female
can become either.
In a few ants, such as Pheidole, this is determined in the egg
stage by the contents of the egg provided by the queen.
In most cases caste fate is determined in the larval stage by the
quantity and quality of food given to the larva. Because
queens are generally larger than workers, this gives the
workers the ability to control the caste of the larvae, and to
avoid too many developing as queens.
In Melipona stingless bees queens and workers are the same
size and reared in the same cells. This gives the larvae the
ability to choose their own caste fate. This leads to more
larvae developing as queens than is needed by the colony. The
excess are executed soon after emerging from their cells.
Queen Not Larger than Worker
Melipona beecheii
Queen
Worker
Queen and worker are the same size although different morphologically.
Note smaller head and lack of pollen basket in queen.
Melipona beecheii Brood Comb
A brood comb in which the cell cappings have been removed to show
queen (circled) and worker pupae being reared in the same cells.
Stages in the Loss of
Worker Reproductive
Potential
Stages in Loss Worker Reproductive Potential
Q-W
morph.
differences?
Q-W caste
determination
1. no
behavioural, equal to queen (no loss ants: queenless Ponerinae
in adult
of reproductive
wasps: Stenogastrinae,
stage
potential)
Polistinae, Microstigmus
bees: Halictidae, Allodapini
2. yes
Developmental
Potential worker
reproductive capacity
Examples
partial loss of reproductive capacity, but
retain ability to mate
ants: some Ponerinae
wasps: some Polistinae
bees: some Allodapini
3. yes
lower than queen;
workers retain ovaries
but cannot mate
ants: most species
wasps: Vespinae
bees: most eusocial Apidae
4. yes
zero; have vestigial
ovaries and so cannot
reproduce directly
ants: a few genera, e.g. Atta,
Monomorium
wasps: none
bees: a few Meliponinae
Stage 1. Paper wasps, Polistes
Female castes (queen, worker) not morphologically distinct.
Ancestral situation. Found in some bees and wasps.
Stage 2. Dinoponera ants
Female castes (queen, worker) not morphologically distinct, all can potentially be queen, but individual females cannot found nest on their own.
Stage 3. Many Species
Bombus terrestris
bumble bee
Lasius niger
pavement ant
Vespula vulgaris
common wasp
Female castes (queen, worker) morphologically distinct. Workers retain
ovaries but cannot mate so can only lay male eggs. This is by far the
most common stage and also includes bumble bees, most stingless bees,
Vespinae wasps, and most ants.
Stage 4. Atta Leafcutter Ants
queen
workers
Female castes (queen, worker) morphologically distinct. Workers have
vestigial or non-functional ovaries and so cannot lay eggs. Found in a
few genera of ants including Atta leafcutter ants and Pharaoh’s ant
Monomorium pharaonis and stingless bees. Also in higher termites.
Some Other Points
Apis mellifera Worker-Laid Eggs
Workers lay many eggs in queenless colonies. In the honey
bee less than 0.1% of the workers in a colony with a queen
have active ovaries, versus up to 50% in queenless colonies.
Specialized Queens
Eciton army ant queen. Army ants have queens specialized for
walking and great fecundity. They are wingless as a new
colony is founded not by a dispersing queen but by colony
fission. Aftican army ant queens, Dorylus, can lay as many as
20,000 eggs per day.
Queens Fighting
Honey bee queens are famous for fighting, trying to kill each
other with their sting. During swarming several new queens
are reared but only one can inherit the colony. A queen cannot
found a nest on her own. As a result they fight.
Worker Morphological Castes
In some species of ants
and termites, the workers
can vary greatly in size.
We will discuss this in the
lecture on division of
labour