C1139 Social Insects. Sex Allocation. Lecture 9
Sex allocation: predictions and tests
Aims
1. To show how to use theory to determine worker-optimum and queen-optimum sex-allocation ratios.
2. To show how these predictions have been tested empirically.
3. Understand some mechanisms by which queen and workers may be able to influence their colony’s sex
allocation, and the final outcome of the conflict.
Objectives
1. Learn how to determine worker-optimum and queen-optimum sex allocation ratios.
2. Learn some of the key studies that have tested sex allocation predictions in social Hymenoptera.
Big picture
The study of sex allocation is one of the most important areas of evolutionary biology in which predictions
from theory are developed and tested. Sex allocation is under strong selection, and there are many situations
in which sex ratios that deviate from even are expected. Social Hymenoptera are arguably the most
important group for the study of sex allocation. Trivers and Hare’s (1976) study of sex allocation in ants
was the most important test of inclusive fitness theory that had been made up to that time, and their results
also changed the way insect societies are viewed. They showed that conflict occurs within insect societies
and that it may well be the workers, not the queen, who are in charge. Studies of facultative sex allocation,
in which workers adjust their colony’s sex allocation according to the type of colony, show the
sophistication of the workers' indirect reproductive strategies and provide further tests of inclusive fitness
theory. Recent studies show that the queen may use some interesting tactics to regain full or partial control
of sex allocation, such as by laying few female eggs to rear into queens so that the workers are forced to rear
males.
Predictions from the theory
We can use inclusive fitness theory to determine the worker-optimum sex-allocation ratio in a population of
social Hymenoptera. We start with the simplest situation in terms of kinship. A population in which all
colonies have the same kin structure: a single mother queen mated to a single unrelated male, with all males
being the queen’s sons.
At the worker-optimum sex-allocation ratio, males and queens have equal kin value to the workers.
(If this were not the case, then workers should invest more in the sex that is worth more to them.)
males
regression relatedness of workers (donors) to
0.5
sex specific reproductive value
1
sex specific reproductive value x regression relatedness 0.5
queens
0.75
2
1.5
In terms of reproductive value and regression relatedness the queens are worth three times as much to donor
workers as the males. Therefore, for the kin value of males and queens to be equal, a unit of allocation to
males must have three times the mating success of the same allocation to young queens. This will occur
when the allocation to females is three times the allocation to males (F/M = 3; 3F:1M; 75% female 25%
male) where F, M are the proportions of allocation to reproduction to females and males in the whole
population.
This result leads to a clear conclusion. Workers should cause a female-biased sex-allocation ratio.
The queen optimum, however, is an equal sex-allocation ratio. You can see why this is so by examining the
table below, in which the regression relatedness of the mother queen to her sons and daughters are used,
instead of relatedness of workers to brothers and sisters.
males
regression relatedness of mother queen (donor) to
1
sex specific reproductive value
1
sex specific reproductive value x regression relatedness 1
Testing theoretical predictions
Trivers & Hare 1976
1
queens
0.5
2
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C1139 Social Insects. Sex Allocation. Lecture 9
In a data set of 21 monogynous (single queen per colony) ant species the sex-allocation ratio was
significantly more female biased than equality (M = F) suggesting worker control.
In 5 Leptothorax ant species the two slave-maker species had approximately even sex-allocation,
and the three non-slave-maker species had female-biased sex-allocation ratios. Trivers and Hare viewed this
as strong support for the idea that workers normally control sex allocation. The slave makers were the
exception that proves the rule. The workers do not rear the brood in slave maker species but instead capture
slaves (pupae of other species) who do the brood rearing and foraging. Because these slaves are unrelated to
the brood they rear they gain nothing by altering the sex ratio. Thus, the queen can win the sex ratio battle
with the workers. Her own workers don’t rear the brood, and the slaves are not selected to oppose her.
Alexander & Sherman 1977
Shortly after Trivers and Hare, Alexander and Sherman said that the female-biased sex-allocation ratio
reported by T&H was due not to worker control, but due to queen control under "local mate competition"
(LMC). LMC means that males compete locally for matings with their brothers. Under LMC, the best sex
ratio for the mother to produce is female-biased. However, for a 3:1 ratio mating must be very local, with
male ants competing not panmictically but with those of only 1-2 additional mother queens. (The most
extreme form of LMC is where all females are mated to their brothers. In this situation we often see highly
female-biased sex ratios, with a mother producing one or two sons, and the rest daughters. In this way, the
mother has more sets of grandoffspring.)
Nonacs 1986
Nonacs reviewed the data all over again and found that it supported T&H not A&S. In particular, he showed
that the sex-allocation ratios of individual colonies are bimodal, which is called "split sex ratios" or “sex
ratio specialization”. LMC does not predict this. Under LMC each colony should produce approximately the
same proportion of males. Nonacs also showed that the sex-allocation ratio is less female biased in
polygynous species (those that have multiple queens per colony). This also supports the inclusive fitness but
not LMC predictions. If LMC was all important, then the sex-allocation ratio would be the same in
monogynous and polygynous colonies.
Further predictions from theory: facultative sex allocation
So far we have only considered the case where all colonies in the population have the same kin structure.
What happens if the kin structure varies among colonies? For example, colonies are headed either by a
single or a multiple-mated queen, or colonies are headed by either one or several queens, or colonies are
headed by either a mother queen or a sister queen. Such situations occur in social Hymenoptera, and in each
case the workers in the first type of colony are selected to rear a more female-biased brood than the workers
in the second type of colony, PROVIDED THAT THEY CAN ASSESS THE SITUATION AND
RESPOND FACULTATIVELY. The calculation shown below shows that the kin value of brothers to
workers is the same in colonies with a single-mated or double-mated queen. But sister queens are worth
more if the mother queen is single mated, and less if she is double mated.
single-mated-queen colony
double-mated-queen colony
females, bfwVF
0.75 x 2 = 1.5
0.5 x 2 = 1
males, bmwVM(mat. suc. males/mat. suc. females)
0.5 x 1 x 2.5* = 1.25
0.5 x 1 x 2.5* = 1.25
* relative mating success of males to females is 2.5 if workers completely control sex allocation, and 50%
colonies are headed by a double-mated queen and 50% by a single-mated queen.
mother-queen colony
sister-queen colony
0.75 x 2 = 1.5
0.375 x 2 = 0.75
0.5 x 1 x 1.8* = 0.9
0.75 x 1 x 1.8* = 1.35
* relative mating success of males to females is 1.8 if workers completely control sex allocation, and 50%
colonies are headed by a mother queen and 50% by a sister queen.
Mueller 1991
Mueller studied the bee Augochlorella striata (Halictidae: Halictinae: Augochlorini), a small metallic green
bee, in New York State. In the spring, lone females build nests in the ground. The founder female (mother)
rears the first brood (females/workers), who then rear the second brood (males and females/queens). The
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C1139 Social Insects. Sex Allocation. Lecture 9
mother sometimes dies. If this is happens she is replaced by one of her daughters. (This species does not
have morphological queen and worker castes.) In this way, the queen can be either the mother or a sister
(i.e., a replacement queen) to the workers. Colonies headed by mother queen produce a more female-biased
sex-allocation ratio than those headed by a sister queen, as predicted by inclusive fitness theory.
Sundström 1994
Studied a species of wood ant, Formica truncorum, in Finland. Colonies have one queen, who can be mated
to one male or several, usually two or three. On average, colonies headed by a double-mated queen have a
more male-biased sex-allocation ratio, as predicted by inclusive fitness theory. Amazingly, this study means
that workers can figure out quite accurately how many times their mother queen mated, probably by
assessing the phenotypic diversity of the female offspring in the colony for some trait where phenotypic
diversity is caused in large part by underlying genetic diversity (different alleles).
Sundström et al. 1996
Studied another wood ant, Formica exsecta, in Finland. As in F. truncorum colonies with a single-mated
queen produced more males. In this study the primary sex ratio (eggs) was also measured, in addition to the
final sex ratio (pupae). In the colonies headed by a single-mated queen there was a significant increase in the
proportion of females from egg to pupal stage (43% to 69%). In the colonies headed by a multiple-mated
queen there was a decrease in the proportion of females (36% to 21%). However, this was not statistically
significant.
Evans 1995 (not shown in slides)
Studied the ant Myrmica tahoensis from Colorado. In about half the colonies workers and young queens are
full sisters and so are offspring of one queen, whereas in the other colonies they are the offspring of two or
more queens. Sex-allocation is more female biased in the former colonies, as predicted by inclusive fitness
theory. Evans also put larvae from several colonies into one monogyne colony. These colonies had a lower
allocation to females. This showed that workers do not count queens to determine kin structure.
Passera et al 2001
Studied the fire ant Solenopsis invicta, a pest species introduced into the USA from Argentina. Fire ant
queens only mate to a single male, and colonies typically have just one queen. In other words, all colonies
have the same kin structure. Nevertheless, some colonies specialize in males and some in females. Why is
this? It seems that it is because some queens lay mainly male eggs. These queens force the workers to rear
many males, even if the workers would rather rear more queens. There are insufficient female eggs to rear
into all the queens and workers that the workers would like to rear. For the workers, rearing more males is
the best of a bad job. This study shows an ongoing conflict between queen and workers.
The more you are losing the more you may gain
Who will win the sex ratio battle between queen and workers? Queen or workers? It is likely that neither
will win. Both parties have some power over the outcome. Queens can manipulate by the number and sex of
eggs they lay. (A queen can control the sex of her eggs by releasing or not releasing sperm.) Workers can
manipulate by the larvae they choose to rear. At the worker-optimum sex-allocation ratio (3F:1M) a unit of
allocation to males and queens is worth the same to the workers. But a unit of allocation to males is worth
three times as much to the queen. So the queen would manipulate sex allocation even at considerable cost to
the colony. That is, she would trade of up to 3 units of queens for 1 unit of males. Similarly, at the queenoptimum sex-allocation ratio (1F:1M), the workers would trade off 3 units of males for 1 unit of young
queens. So the more you are losing, the greater incentive you have to manipulate and the greater the cost to
the colony you will be willing to sacrifice in doing this.
*Alexander, R. D., Sherman, P. W. 1977. Local mate competition and parental investment in social insects. Science 196: 494-500.
Boomsma, J. J., Grafen, A. 1991. Colony-level sex ratio selection in the eusocial Hymenoptera. J. Evol. Biol. 3: 383-407.
Bourke, A. F. G. 1989. Comparative analysis of sex-investment ratios in slave-making ants. Evolution 43: 913-918.
*Evans, J. D. 1995. Relatedness threshold for the production of female sexuals in colonies of a poygynous ant, Myrmica tahoensis, as revealed by
microsatellite DNA analysis. Proc. Natl. Acad. Sci. USA 92: 6514-6517.
Helanterä, H., Ratnieks, F. L. W. 2009. Sex allocation conflict in insect societies: who wins? Biology Letters 5:700-704.
*Mueller, U. G. 1991. Haplodiploidy and the evolution of facultative sex ratios in a primitively eusocial bee.Science 254: 442-444.
*Nonacs, P. 1986. Ant reproductive strategies and sex allocation theory. Q. Rev. Biol. 61: 1-21.
Ratnieks, F. L. W. 1990. Assessment of queen mating frequency by workers in social Hymenoptera. J. Theor. Biol. 142: 87-93.
Ratnieks, F. L. W. 1991. Facultative sex allocation biasing by workers in social Hymenoptera. Evolution 45: 281-292.
Ratnieks, F. L. W., Boomsma, J. J. 1995. Facultative sex allocation by workers and the evolution of polyandry by queens in social Hymenoptera.
Am. Nat. 145: 969-993.
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C1139 Social Insects. Sex Allocation. Lecture 9
**Ratnieks, F. L. W., Wenseleers, T., Foster, K. R. 2006. Conflict resolution in insect societies. Annual Review of Entomology 51: 581-608.
*Sundström, L. 1994. Sex ratio bias, relatedness asymmetry and queen mating frequency in ants. Nature 367 266-268.
*Sundström, L., Chapuisat, M., Keller, L. 1996. Conditional manipulation of sex ratios by ant workers: a test of kin selection theory. Science 274:
993-995.
Sundström, L., Ratnieks, F. L. W. 1998. Sex ratio conflicts, mating frequency and queen fitness in the ant Formica truncorum. Behavioral Ecology
9:116-121.
*Trivers, R. L., Hare H. 1976. Haplodiploidy and the evolution of the social insects. Science 191: 249-263.
* papers referred to specifically in handout; ** recent review of sex-allocation conflicts and all conflicts over reproduction in insect societies
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