Behavioral Ecology Vol. 9 No. 2: 116-121
Sex ratio conflicts, mating frequency, and
queen fitness in the ant Formica truncorum
Iiselotte Sundstrom* and Francis L. W. Ratnieksb
•Department of Genetics and Ecology, University of Aarhus, DK-8000 Aarhus C, Denmark, and
b
Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK
We examined the effect of facultative sex allocation by workers on queen fitness in a Furnish population of the ant Formica
truncorum. Workers rear female-biased broods in colonies headed by a singly mated queen and male-biased broods in colonies
headed by a multiply mated queen. As a result, multiply mated queens have a 37% fitness advantage over singly mated queens.
Neither reproductive output nor worker population of colonies varied with queen mating frequency. We suggest that singly
mated queens persist in the population because fitness benefits to multiply mated queens via sex allocation are balanced by
costs of additional mating*. Alternatively, singly mated queens may persist simply because some queens lack opportunities to
mate multiply or because male control sometimes prevents additional matings by queens. Kty words: eusodah'ty, Formica, queen
fitness, sex allocation, social insects, worker-queen conflict. [Behav Ecol 9:116-121 (1998)]
T
he costs and benefits of mating with multiple partners are
major factors in the evolution of animal mating systems
(Thornhill and Alcock, 1983). Benefits to males are obvious,
because having multiple partners readily translates into more
offspring. Benefits to females are not obvious, particularly in
species where males provide no parental care or other resources, or where females need to mate with only one male
to ensure their fecundity.
In social Hymenoptera, queens mate early in adult life. Remating rarely occurs, possibly only under laboratory conditions (Rosengren et al., 1993), and sperm stored in a queen's
spermatheca remain viable for the life of the queen, up to 30
years in some ants (Pamilo, 1991). In fact, the life span of a
queen may directly depend on the availability and viability of
the sperm stored, and several studies have shown that multiply
mated queens have more sperm than singly mated ones (Fjerdingstad, 1996; Fortelius 1994; Rdseler, 1973). In ants, queen
mating frequency varies from exclusively one (e.g., Soienopsis,
in two species the mean effective paternity frequency is 1.0),
from one to a few (e.g., Formica; in six species the mean varies
between 1.03 and 1.48) to almost always greater than one
(e.g., Atta colombica, the mean is 1.96) (Boomsma and Ratnicks, 1996; Fjerdingstad et al., 1997).
Several hypotheses have been put forward to explain how
a queen's fitness may be affected by her mating frequency
(Crozier and Page, 1985; Crozier and Pamilo, 1996). The*e
can be classified as: (1) queen fecundity: mating frequency
influences the number of sperm stored and hence maximum
fecundity. As a result, multiply mated queens may have a longer reproductive life than singly mated queens because they
have more sperm; (2) colony performance: mating frequency
influences the genetic diversity of the queen's diploid offspring (workers, new queens, and diploid males), which in
turn may affect colony survival and efficiency; and (3) facultative sex allocation. The three hypotheses are not mutually
exclusive, and they all predict a fitness advantage for multiple
mated queens.
L. StmdstrOm ts now at the Department of Ecology and Systematic*,
Helsinki University, PO Box 17, FIN-00014 Helsinki University, Finland.
Received 24 February 1997; first revision 5 June 1997; second revision 15 July 1992; accepted 16 July 1997.
O 1998 International Society for Behavioral Ecology
Facultative sex allocation is a strategy in which a colony's
workers preferentially rear the sex that is of greater value to
them (Boomsma and Grafen, 1991; Ratnieks and Boomsma,
1997). When colonies each have a single queen and queens
are inseminated either singly or multiply, workers can enhance their inclusive fitness by preferentially rearing females
in colonies headed by a singly mated queen and males in
colonies headed by a multiply mated queen (Boomsma and
Grafen, 1991). Such facultative sex-ratio biasing also affects
the fitness of the mother queen (Ratnieks and Boomsma,
1995). A queen is equally related to her sons and daughters,
so from her perspective the value of males will increase when
worker control results in female-biased populationwide sex ratios (Crozier and Pamilo, 1996; Trivers and Hare, 1976). Even
when workers make errors in assessing queen mating frequency, multiply mated queens more frequently head malebiased colonies than do singly mated queens and therefore
have a fitness advantage over singly mated queens (Ratnieks
and Boomsma, 1995).
Theory suggests that facultative sex allocation by workers
can select for multiple mating by queens (Ratnieks and
Boomsma, 1995). In a population with mixed single and double mating, the maximum fitness difference due to sex allocation between doubly mated and singly mated queens that
have successfully established a colony varies from 3-fold to
1.33-fold, depending on the proportion of doubly mated
queens in the population (Ratnieks and Boomsma, 1995).
Benefits of multiple mating decrease if workers make errors
in assessing queen mating frequency, if some males are workers' sons, if colony sex ratios are less extremely bimodal than
the worker optimum or if the populationwide sex ratio is less
female-biased than the worker optimum (Boomsma and Grafen, 1991; Ratnieks and Boomsma, 1995, 1997).
In this study we quantified the effect on queen fitness
caused by facultative sex allocation by workers in response to
variation in the mating frequency of their mother queen. We
did this by assessing the relative fitness of singly mated and
multiply mated Formica truncorum queens using field data
from a Burnish population is which facultativs soxrfstio biasing by workers occurs (Sundstrom, 1994). Importantly, some
colonies have been followed during the entire period of study
and have shown little variation in sex allocation ratios (Sundstrom, 1994,1995b, unpublished data). This suggests that agedependent changes in colony sex ratios are uncommon and
117
Sundstrom and Ratnieks • Queen fitness in ants
TaMel
Average aex ratios and queen fitness (i
Sex ratio (% females)
Queen fitness
No. of
reproductive*
No. of workers
1989-91
if
1992-95
if
1992-95
1992-95
n
Colonies headed by singly-mated queens
0.75 2t0.34
\fearl
0.84 2•0.24
2
0.76:t 0 .33
0.77 2i 0.38
0.79:i 0.31
3
0.80 2= 0.29
Mean
0.77 2t 0.31
0.80 2t 0 JO
1.86 2t 0.38
1.85 2tOJ7
1.83 2•0.33
1.85 2i 0.35
8(9)
8(9)
8(11)
1.74 i 0.38
1.88 ± 0.22
1.88 t 0.85
1.83 * 0.34
10(11)
10 (14)
10 (13)
4274* 2073
1151 ± 916
3492 ± 2276
2975 ± 2241
9493
6998
8171
8221
:t 5986
:t 3255
:t 3539
2t 4401
10
10
10
Colonies headed trf doubly
0.15 2t 0.31
Year 1
2
0.18 2t 0.33
3
0.23 2i 0.34
Mean
0.19 2t 0.32
2.53 2t 035
2J51 2tO.37
2.49 2t 0.38
2.50 2: 0 J 5
8(8)
8(8)
8(10)
2.47
2.21
2.87
2J2
4270
3371
3183
3690
9176 2t4624
6363:i 2772
6110 2t 3140
7400 2tS851
8
6
7
1989-91'
1992-95*
± SD) in 1989-91 and 1992-95 and number of adub workers and sexual production in 1992-95
mated queens
0.38 i: 0 J 2
0.15 2= 0.29
0.43 2: 0.42
0 J 2 i:0.35
• 0.42
i 0.14
i 0.99
± 0.66
8(11)
8(9)
8(10)
+ 2718
i 1494
• 2760
± 2760
* Based on average values, without correction for productivity differences among colonies.
With correction for productivity differences among colonies (Bourke and Franks, 1995).
c
Numbers in brackets give the total number of live colonies in the year of sampling.
b
that each colony consistently produces either a male-biased or
female-biased sex ratio over several years. For the same reason, sperm depletion seems an unlikely cause of male bias
because if no new workers are produced the colony will die
within a year. Nevertheless, colonies headed by multiply mated
queens produced male-biased sex ratios during several consecutive years.
METHODS
Study
rtr
g*'^»*gi1
The study population of F. truncorum is located on six adjacent islands in southwest Finland (Sundstrom, 1994, 1995b).
Thirty nests were censused between 1989 and 1995. The data
for 1989-1992 have been published (Sundstrom, 1994,
1995b), but those for 1994-1995 are new. Because some colonies died or were newly founded during the study, the number of colonies censused varied, but averaged 16 per year. The
total number of active colonies averaged 20 per year (Table
1). Hence, on average 80% (range 70-100%) of the entire
population was censused each year. Colonies are conspicuous
and immobile, so the entire population can be censused and
individual colonies followed year to year. Genetic studies have
shown that the population is largely panmictic and that each
nest has a single queen (Sundstrom, 1993). Colony sex allocation ratio, production of new queens and males, and worker
population were estimated using mark-recapture methods
(Sundstrom, 1995b). Queen mating frequency was determined by analyzing worker genotypes at polymorphic allozyme (Sundstrom, 1993, 1994) and microsatellite DNA loci
(Chapuisat, 1996). Following the use of microsatellites, one
queen previously classified as single mated (Sundstrom, 1994)
was found to be double mated (Gertsch P, personal communication), and is here included in the multiply mated category. The large amount of allozyme and microsatellite variation results in a negligible probability, 0.7%, of misclassifying
a multiply mated queen as single mated due to identical paternal genotypes at all loci.
Based on year-to-year consistency of nest location and worker genotypes, some queens heading the study nests are known
to have lived at least 9 years (Sundstrom L, unpublished data).
In F. exsecta the average life span of a queen was estimated at
30 years (Pamilo, 1991). The great longevity of Formica
queens in single-queen nests makes it impractical to calculate
queen fitness over the entire queen life span. Nevertheless,
our data cover 6 study yean over a 7-year period. The colonies
that have been followed during the entire study period show
little year-to-year variation in sex allocation ratios (Sundstrom,
1994,1995, unpublished data), suggesting that age-dependent
changes in sex ratios are of minor importance.
Data on colony sex-allocation ratios were collected for 6
years, and data on worker population and number of queens
and males produced were collected for 3 of these years. We
therefore divided our data into two groups: one where only
sex ratios were measured (1989-1991) and one where sex ratios, worker population, and sexual production were measured (1992-1995). No data were collected in 1993. Because
some colonies died or were newly founded, the identities of
the colonies studied in the two 3-year periods are not entirely
overlapping. For die analysis of sex ratios and queen fitness
we only included colonies for which data were available for
all 3 years, 1989-1991 or 1992-1995, or both. For the analysis
of worker population and sexual production, we used the
same set of colonies. However, productivity and worker population data were available only for 1 or 2 years in some of
these colonies. This resulted in missing values that were replaced by estimates (see below).
In 1992-1995 populationwide sex ratios were estimated directly by summing the male and queen production of individual colonies (Sundstrom 1995b). Sexual production were not
measured in 1989-1991. Instead we used die arithmetic mean
of the population sex-allocation ratios in years 1992-1995 as
an estimate.
Calculation of t»wln»iw» fitness
In a large panmictic population, the inclusive fitness, Wv of
a queen can be expressed as
W q - N(bmqVam/M+
b^VJ/F),
(1)
where N is die total allocation to reproduction, bm^ and
are the regression relatedness of the queen to the male an
female reproductives produced in her colony, Vm and V, are
the reproductive values of males and females, m (= 1 — fi
and / are die proportional allocation to male and female
reproductives in individual colonies, and Af ( = 1 — F) and F
are die proportional allocation to male and female reproductives in die population. (For details see Crozier and Pamilo, 1996.)
Behavioral Ecology Vol. 9 No. 2
118
Tablet
ANOVA of <U£F<
among colonies in worker populatki
Years
Mates (Af)
tear (r)
F
df
F
1.14
1.14
2J6
2.66
1.16
1.16
1.15
1,15
1.86
1.07
6.22
2.15
p
1989-91
Sex ratio
Queen fitness
12.7
12.8
1992-95
Sex ratio
Queen fitness
No. of reproductives
No. of workers
25.9
<.0001
7.87
.013
1.0
>.10
0.28
>.10
M * colony
Error term
I production, aexratio,and queen fitness per year and mating
.003
.003
Interaction (Y* M)
P
df
F
P
df
>:!S
2,2
2,2
1.10
0.20
>:JS
2,2
2,2
2.2
2,2
0.35
1.79
1.27
0.71
2,28
2,28
2.32
2,32
2,30
2,30
.01
Y* C
M* Y*
c
Significances are based on exact F tests, with degrees of freedom given for both the main effect and the error term.
Worker production of males affects h^ and the ratio \fc Vm.
In queenright colonies both genotype distribution* and relatedness coefficients strongly suggest that worker reproduction
does not occur (Sundstrom 199S, Walin L, Sundstr&m L, Seppa P, and Rosengren R, submitted manuscript). Another
source of worker reproduction is orphaned nests. During the
entire study period seven colonies died. Two produced only
males during their last season, whereas the other five had no
phase of exclusive male production before death. In the two
colonies that produced males only, no change in male genotypes occurred between the penultimate and final years. This
strongly suggests that worker reproduction is negligible in orphaned colonies and in the population as a whole. Hence, V,
= 2Vm, ifc, - 0.5. and h^ - 1, so that b^Vf - bax>Vm - 1
(setting Vr - 2; cf. Pamilo, 1991).
The total production of reproductives did not differ significantly between colonies headed by singly mated or multiply
mated queens (see below). Therefore, Equation 1 simplifies to
W^ -
( H I / M ) + (X/F),
(2)
in which the subscript i refers to a specified queen or her
colony. Equation 2 was used to calculate the inclusive fitness
of singly and multiply mated queens using the populationwide
M and .F values for each year in 1992-1995, or their estimates
in 1989—1991, and the m and/values per colony per year for
each year.
Statistical analyses
Parametric tests were used after confirming that all dependent variables WCTC normally distributed (Wilk-Shapiro rankit
plot r > 0.9). We used two-way ANOVAs to test the effects of
mating frequency and year on queen fitness (1989-1991 and
1992-1995), sexual production and number of adult workers
(1992-1995 only). The same colonies were used in different
years, hence colonies were entered as randomized blocks within each mating class and year (split-plot design). Because the
set of colonies used in 1989-1991 and 1992-1995 were not
completely overlapping, these periods were analyzed separately to avoid too unbalanced a design. For the 1992-1995 data
the design was still slightly unbalanced, and to overcome this
we replaced the missing values (six for sex ratio and queen
fitness analyses, nine for colony size and productivity analyses)
with the yearly average (Sokal aad Rohlf, 1995). Exact F tests
were constructed to test significances.
RESULTS
Table 1. gives, per mating class, the average sex allocation ratio, queen fitness, number of reproductives produced, and
number of adult workers. The average populationwide sex ra-
tios expressed as the proportion of females, F (Af = 1 - F)
were 0.67 in 1992, 0 3 7 in 1994, and 0.76 in 1995, yielding a
mean of 0.67± 0.095 (SD). The mean value of 0.67 was used
as an ***i*M't* for the populationwide sex-allocation ratio in
1989-1991.
Neither the number of reproductives produced nor the
number of adult workers per colony differed significantly between singly mated and multiply mated classes (Table 2). The
number of reproductives produced varied significantly between years, whereas the number of adult workers did not
(Table 2, Figure 1). A pairwise comparison of worker population between years gave no significant differences between
any pair of years for the singly mated class ( ^ ^ « 1.3, df ™
9, p > .10), whereas one pair of years, 1992 and 1994, differed
significantly for the multiply mated class (tWMX « 2.87, df «• 5,
p " .035). However, this difference was not significant following Bonferroni correction for multiple comparisons (/>>.10).
Because colony productivity did not differ between the two
classes, no productivity correction was needed.
Both colony sex ratio and queen fitness differed significantly between mating classes (Table 2, Figure 1), with an
average fitness ratio ( H ^ / W y of 1.37 (±0.11, SD). Thus
the difference in sex allocation ratios between colonies headed by singly mated and multiply mated queens gives a 37%
fitness advantage to multiply mated queens.
Of the 30 colonies studied 17 were headed by a singly mated queen, 10 by a doubly mated queen, and 3 by a triply
mated queen. The paternity contribution of third males was
invariably low, and the effective paternity frequency of triply
mated queens about two (Walin L, Sundstrom L, Seppa P.
Rosengren R, submitted manuscript). During the study seven
colonies died—three headed by a doubly mated queen and
four by a singly mated queen. This suggests that colony mortality does not strongly depend on queen mating frequency
(Fisher's Exact test, p «* 1.0). Of four newty founded colonies,
two each were headed by singly mated and doubly mated
queens.
DISCUSSION
Possible factors w»
Facultative sex allocation by workers results in an average
37% fitness advantage to multiply mated F. truncorum
qtleeTW compared to singly mated queens. The disadvantage of single mating was not compensated by higher colony productivity or higher colony survival of colonies headed by singly mated queens. If anything, productivity seemed
lower in colonies headed by singly mated queens. Hence,
the 37% fitness advantage is most likely a minimum estimate, and the multiply mated queens may have additional
Sundstrom and Ratnieks • Queen fitness in ants
• • Singly mated
I—I Multiply mated
119
B
1500O-
1
10000-
5000-
1992,94-96
1989-91
T
tttl
fitness gains through higher colony productivity. Given this
substantial advantage, why are singly mated queens a frequent phenomenon?
The proportions of singly mated and multiply mated
queens in the population may reach an equilibrium where
benefits from multiple mating are balanced by costs of multiple mating (Ratnieks and Boomsma, 1995). Importantly, the
fitness benefits of multiple mating decline with increasing proportions of multiply mated queens in the population. This is
because male-bias colonies become the balancing class and
workers in them are selected to produce both males and females (Boomsma and Grafen, 1991; Ratnieks and Boomsma,
1996). For example, the maximum fitness advantage of doubly
mated queens drops from 3:1 to 1.33:1 as their proportion
increases from 25% to 100% (Ratnieks and Boomsma, 1995).
This decline still occurs when workers make errors in assessing
queen mating frequency (Ratnieks, 1990). The frequency of
doubly mated queens could thus increase from an initially low
level until the costs and benefits are equal. Costs of multiple
mating may arise through increased risks of predation, injury,
or disease transmission during longer nuptial flights. In some
Formica ants, queen mortality during nuptial flights apparently is high (O'Neill, 1994).
Alternatively, single mating may prevail because some
queens are unable find a second mate. In F. truncorum females outnumber males because the populationwide sex allocation ratio is female-biased, and females and males have
approximately equal weights (Sundstrom, 1995a). Combined
with the short life span of male ants, a relative shortage of
males may arise. Thus, females may be unable to remate because males are hard to find.
Single mating by queens could be partly a result of male
mating tactics (Boomsma, 1996). Sexual selection theory predicts that the more limiting sex will be choosier (Andenson,
1994). Males may reject mated females if virgin females are
easily available and males are sperm limited. This is because
a second male will likely father only a fraction of a multiply
mated queen's daughters. This effect is even stronger in ants
with facultative sex allocation because colonies headed by
multiply mated queens produce male-biased sex ratios. When
Figure 1
Variation (mean ± 95% Q)
among colonies in (A) worker
population, (B) sexual production, (C, D) queen fitness per
year and mating class.
a colony's males are the queen's sons, they are unrelated to
the queens' mates. Thus, males may benefit from preventing
their mates from subsequent matings. Potential male control
methods, such as mating plugs or mate guarding, have not
been reported in Formica. However, Formica males could exercise some control by pheromonally marking queens during
copulation. Second males would then be able to easily recognize virgins from nonvirgins.
Factors decreasing die fitness advantage of multiple ""*i"g
In the study population the effective paternity is 1.43 and
mean sperm bias is 0.33:0.67 (Sundstrom, 1993). Given these
values, the theoretical maximum fitness advantage of multiply
mated queens over singly mated queens is approximately 75%
(Ratnieks and Boomsma, 1995). Several factors might cause
the observed fitness advantage of multiply mated queens
(37%), to be lower than this.
The population-wide sex allocation ratio may be less female
biased than die worker optimum, so that die fitness benefits
from producing males are lower. Given the observed effective
paternity, the worker-optimum populationwide sex-allocation
ratio is 67% females (Boomsma and Grafen, 1991), which
closely matches the observed average value, 0.67±0.095. Unequal sperm use and errors in the assessment of queen mating
frequency raise this value only slightly (Ratnieks and Boomsma, 1996).
Workers may respond to factors in addition to queen mating frequency when optimizing colony sex ratio. In the
study population there is a positive correlation between colony productivity and female allocation, with productivity
explaining 23% of colony sex-ratio variation (Sundstrom,
1994, 1995b). Small colonies headed by a singly mated
queen produced some males, and large colonies headed by
a multiply mated queen produced some females, thus decreasing the fitness differences between singly and multiply
mated queens (Boomsma and Grafen, 1991; Ratnieks and
Boomsma, 1995).
Workers in some colonies may assess queen-mating frequency incorrecdy. Given the observed mating frequencies
120
Behavioral Ecology Vol. 9 No. 2
Singly mated
Multiply mated
Figure J
Yearly colony-specific sex allocation ratios of the colonies included in this study. Note that
the set of colonies presented
here is not identical to that in
Sundstrdm (1994).
0.0-0.2
0.4-0.6
0.8-1.0
0.2-0.4
0.6-0.8
0.0-0.2
0.4-0.6
0.8-1.0
"
0.2-0.4
0.6-0.8
0 0-0 2
0.4-0.6
0.8-1.0
0.2-0.4
0.6-0.8
0.0-0.2
0.4-0.6
0.8-1.0
0.2-0.4
0.6-0.8
0.0-0.2
0.4-0.6
0.8-1.0
0.2-0.4
0.6-0.8
* 0.0-0.2
0.4-0.6
0.8-1.0
0.2-0.4
0.6-0.8
the singly mated class of colonies is expected to produce exclusively females and the multiply mated class of colonies both
males and females (Boomsma and Grafen, 1991; Ratnieks and
Boomsma, 1996). Thus, the fitness of singly mated queens is
enhanced if the workers wrongly assess their queen as multiply
mated and rear a male-biased sexual brood, whereas the fitness of multiply mated queens decreases. A few colonies with
singly mated queens produced male-biased broods, but all had
low productivity, so both assessment errors and productivity
correlations equally well explain male bias in these colonies
(Figure 2).
Conduaioaa
Multiply mated queens have a substantial fitness advantage
over singly mated queens, which is approximately half die theoretical maximum. Despite die considerable fitness advantage
of multiple mating, singly mated queens remain frequent in
the population. Sex allocation is probably only one of several
factors-that affect queen fitness, and sax alleaation benefits of
multiple mating may be balanced by costs of additional matings. In die absence of productivity or mortality disadvantages
to established colonies headed by multiply mated queens,
costs of additional matings may maintain variation in mating
frequency. If mating frequency is at an equilibrium of equal
fitness for single and multiply mated queens then copulation
Proportion females
costs must be high to compensate for die 37% fitness advantage via sex allocation to die multiply mated queens. Few data
are available on costs of mating in ants, presumably because
diese are extremely difficult to quantify. Some testable predictions can, however, be made: (1) If male interests limit
opportunities for queens to mate multiply, then mated queens
should be less attractive to males seeking copulations. (2) If
male abundance affects die ability of queens to mate multiply,
then queen mating frequency should be higher in populations where other factors acting in addition to relatedness
asymmetry (such as local resource competition among females) increase male bias, i.e., the populationwide sex ratios
are more male biased than expected based on die frequency
of multiply mated queens in die population alone. (S) Where
costs of additional matings can be estimated, we predict diese
to be high.
We thank Roos Boomsma, Andrew Bourke, Else Fjerdingstad, Laurent
KeiteT and Laura Walin for discussions and commerce on previous
drafts of the paper. Pia Ceruch, Roger Foreman, and Helena Aberg
helped in the field, and the Tvarminne Zoological Station provided
working facilities. Pia Certsch kindly kept L.S. up to date on microsatellite screenings of the colonies. The Danish National Science Research Council and Swiss National Science Foundation provided funding (to l_S.) and the research network "Social Evolution" financed
Sunditrom and Ratnieks • Queen fitness in ants
by the European Commission via the Training and Mobility of Researchers (TMR) programme.
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