Biological Journal of the Linnean Society, 2002, 76, 591–600. With 5 figures
Mitochondrial DNA distributions indicate colony
propagation by single matri-lineages in the social spider
Stegodyphus dumicola (Eresidae)
JES JOHANNESEN*, ANNA HENNIG, BIANCA DOMMERMUTH and
JUTTA M. SCHNEIDER
Institute of Zoology, Ecological Department, University of Mainz, Saarstrasse 21, 55099 Mainz,
Germany
Received 13 December 2001; accepted for publication 10 April 2002
Colony-dwelling social spiders of the genus Stegodyphus are characterized by high colony turnover, within-colony
mating, inbreeding and skewed sex ratios. These phenomena may purge genetic variation from the entire species
gene pool. Social Stegodyphus have previously been discussed as ecologically unstable and evolutionary dead ends.
We investigated the distribution and age (sequence divergence) of mitochondrial DNA variation for inferences of
colony propagation, colony discreteness and maintenance of genetic variation in the social spider S. dumicola. In
contrast to our expectations, we found abundant mtDNA variation, consisting of 15 haplotypes belonging to four
haplotype lineages. Lineage divergence ranged between 2.75 and 6% for the gene ND1. Nearly all colonies (86%)
were monomorphic and even neighbour colonies showed fixed differences. Simulations show that genetic drift in
multifounder colonies cannot alone explain monomorphism within colonies. Haplotypes in polymorphic colonies and
from neighbouring colonies were always genealogically similar. Monomorphism and the genealogical pattern among
colonies suggest ‘clonal’ colony propagation involving single matrilineages. The divergence of haplotype lineages and
distribution of haplotypes imply that colony turnover is not high enough to purge genetic variation in the species
gene pool, and that S. dumicola as a species is old enough to question the instability (in ecological time) of a social
spider. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 76, 591–600.
ADDITIONAL KEYWORDS: mitochondrial DNA – Namibia – propagule dispersal – social spider – population
structure
INTRODUCTION
Genetic and phenotypic variation is maintained by a
balance between mutation, genetic drift, gene flow and
differential selection in subdivided populations or
breeding units. Assuming no mutation, mating within
a population will eliminate variation through genetic
drift, whereas the differential extinction of populations will purge genetic variation at the global level,
ultimately leading to the success of one lineage and
complete monomorphism within the species. The
degree to which loss of variation occurs depends on the
abundance of populations, their turnover rates and
*Corresponding author. E-mail: [email protected]
gene flow among them (Hartl & Clark, 1989; Hedrick
& Gilpin, 1997). Lack of genetic variation will halt the
evolutionary potential of a species (Falconer, 1989;
Wagner & Altenberg, 1996).
Social spiders (non-territorial permanently social
sensu Avilés, 1997) are likely to provide an intriguing
example for investigation of the above processes.
Social spiders live in closed colonies that may have
high turnover rates (e.g. Roeloffs & Riechert, 1988;
Avilés, 1997; Crouch & Lubin, 2001). The mating
system is characterized by inbreeding and skewed sex
ratios. Mating is thought to take place solely within
the parent colony (Avilés, 1997). These characteristics
are associated with processes that decrease effective
population sizes and which may lead to rapid loss of
genetic variation. Allozyme studies have found little
© 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 76, 591–600
591
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J. JOHANNESEN ET AL.
allelic variation in social spiders (see Table 12.5 in
Riechert & Roeloffs, 1993), and that found to be
present is mostly distributed among colonies, implying restricted breeding systems (e.g. Lubin & Crozier,
1985; Roeloffs & Riechert, 1988; Smith & Engel, 1994;
Smith & Hagen, 1996). The mating system in social
spiders thus differs from that of eusocial insects,
which is characterized by premating dispersal and
outbreeding. It has been suggested that the inbred
mating system of social spiders hints at an evolutionary dead end once colony-living behaviour is fixed
(Wickler & Seibt, 1993). Indeed, sociality is rare in
spiders; out of about 30 000 described species of
spiders only 30 or so are considered social (Avilés,
1997).
The social spider Stegodyphus dumicola shows the
population characters typical for social spiders (Seibt
& Wickler, 1988). Sociality in the genus Stegodyphus,
which contains three social species, is thought to have
taken the ‘subsocial pathway’. It implies that siblings
gradually delay dispersal until they have reproduced
as a group. It entails increasing the genetic variance
among breeding groups by means of philopatry or
inbreeding. Analysis of population structure of the
subsocial Stegodyphus lineatus indicated that differentiation among nest clusters is enhanced by
female-mediated group founding coupled with limited
mating-dispersal (Johannesen & Lubin, 1999, 2001).
In S. dumicola, all females are potential breeders
and are believed to mate exclusively within the parent
colony. Afterwards, they disperse, either singly or in
sister groups, and found new colonies. Otherwise,
colonies may divide by budding, i.e. break apart into
new colonies. Thus, the population structure is
thought to be influenced predominately by female
behavioural decisions.
Although the available data on S. dumicola suggest
closed colony structure possible ways of gene flow
cannot be excluded. Wickler & Seibt (1993) reported
allozyme variation in S. dumicola although unfortunately they did not quantify its distribution. Gene flow
could occur through several mechanisms. Neighbouring colonies of different origins may fuse. Furthermore, males may leave their natal colony and join
other groups to mate. Although foundresses are likely
to have mated before dispersal, the percentage of
unmated females is unknown and mated females may
re-mate with males from other colonies. Finally,
groups of females from different origins may found
new colonies together. Adult females may disperse
over short distances by bridging or over farther distances by ballooning (Schneider et al., 2001). Ballooning females of different origin may meet at sites that
are favourable for landing (e.g. trees). None of the
mechanisms described above have been confirmed to
date.
Population genetic studies using allozymes have
provided compelling evidence for restricted breeding
systems in other species of social spiders. However,
genetic homogeneity, on the one hand, and lack of
knowledge of allele genealogy, on the other, has limited
these studies with respect to inferences of colony propagation. In this paper we analyse the distribution
and genealogy of maternally inherited mitochondrial
DNA sequence variation within and among colonies
of S. dumicola and discuss the implications for colony
propagation, colony discreteness and the maintenance
of genetic variation. Assuming strict propagule dispersal, closed colonies and high colony turnover, we
expected only limited mtDNA variation. As we shall
show, however, mtDNA variation is abundant. We
investigate whether mtDNA distributions originate
from single- or multifemale colony founding. If the
distribution originates via the former, we expect
mtDNA monomorphism within colonies, with neighbouring colonies having identical or genealogically
similar haplotypes. Alternatively, monomorphism may
arise due to genetic drift even if unrelated females
generally establish colonies. In simulations, we test
whether drift overrides evidence of repeated multilineage colony founding by varying (1) the number of
founding females (2) time since colonization and (3)
colony size. Finally, considering the age (sequence
divergence) and diversity of S. dumicola haplotypes,
we address, tentatively, the question of evolutionary
flexiblity in a social Stegodyphus. We compare haplotype differences within S. dumicola with those of its
solitary sister species Stegodyphus tentoriicola for
evolutionary species integrity. The latter species is
slightly larger but morphologically similar to S. dumicola. It has been hypothesized that S. tentoriicola
could be solitary S. dumicola (J. Henschel, pers.
comm.).
MATERIAL AND METHODS
Spiders were collected in Namibia between 21
January and 5 February 2000 (Fig. 1). Voucher specimens are deposited at the National Museum in Windhoek, Namibia. To compare colony mtDNA variation
within and among areas we investigated spiders from
23 colonies from seven areas in a hierarchical manner.
Colonies were always sampled from different bushes.
Colonies D–G at Omdraie were situated within a
radius of 50 m, at Rehoboth (S–V) within 100 m, and
at Uhlenhorst (W–Z) within a radius of 50 m. At Dan
Viljong (A, B, C, I), colonies C and I were 10 metres
apart and situated 750 m and 1500 m from colonies
A and B, respectively. At Outjo (J–M) the density of
colonies was low. The colonies J and K were separated
by 400 m. The distances from J to colonies L and M
were approximately 4700 m and 1900 m.
© 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 76, 591–600
mt DNA VARIATION IN A SOCIAL SPIDER
Namibia
Outjo
Dan Viljong
O mdraie
Ga msberg
Rehoboth
Uhlenhorst
Sesriem
250 km
Figure 1. Sampling locations of S. dumicola in Namibia.
Female spiders were transported live to Mainz for
rearing experiments (J. Schneider unpubl.) and afterwards kept frozen at -80 °C until analysis. Males were
conserved in 70% ethanol in Namibia. We sequenced
five to seven individuals from each colony except for
two colonies where only two and three individuals
were collected.
We sequenced a partial mitochondrial sequence (581
characters, including gaps) spanning the ND1 and
16S genes. Previously, the sequence has shown great
intraspecific variability in other spiders (Hedin, 1997;
Johannesen & Veith, 2001). The sequencing protocol
and primers are given in Johannesen & Veith (2001).
Sequences were aligned using the program Sequence
Navigator (ABI). Subsequently, all aligned sequences
and electropherograms were checked manually to
confirm base substitutions. The sequences have
GenBank accession numbers AF 494425–494439.
Differentiation among colonies was quantified by
AMOVA as implemented by Arlequin for haplotypic
data (Schneider, Roessli & Excoffier, 2000) using the
Tamura–Nei (TN) distance model (see below) and traditional frequency distributions. Both estimators are
based on frequency data, but where TN incorporates
divergence among haplotypes, traditional frequency
distributions assumes all haplotypes are equally
divergent. Minimum spanning networks were constructed using Arlequin for within-clade genealogies.
To investigate whether sequence divergence can be
correlated to lineage age we tested for clock-like evolution with PUZZLE 4.02 (Strimmer & von Haeseler,
1996).
593
The interaction between multifemale colony
founders and small population size on within-colony
mtDNA variation was tested with the simulation
program E A S Y P O P (Balloux, 2001). We simulated
variability over expected colony-persistence time (5,
10 and 20 generations). We let colonies start with 2, 3
or 4 founding females. This corresponds to the number
of haplotypes found within a local area. Colony sizes
were 10, 20, and 40 females. Females (i.e. haplotypes)
were allocated randomly to each colony. Colonies
attain carrying capacity in one generation, thereafter
colony size is kept constant. There is no dispersal
between colonies. Each scenario was simulated 100
times. After each simulation we randomly drew six
individuals from every colony. This corresponds to our
sample sizes. Based on these six individuals, we
generated distributions over the expected number of
alleles per colony and the proportion of polymorphic
colonies. The former was tested with Mann–Whitney
U-tests. The latter was calculated for subsets of 20
simulations from which 95% confidence intervals were
calculated. Twenty colonies correspond to the number
of colonies sampled in the present study. A full-grown
colony has perhaps 100–200 females and most colonies
will probably never persist 20 generations without
splitting or dying off. Our drift estimates are therefore
conservative.
Sequence divergence within S. dumicola was compared to its sister-species S. tentoriicola (GenBank
AF 494440) collected in South Africa for inference of
monophyletic assignment of S. dumicola haplotypes.
Stegodyphus lineatus was used as outgroup (GenBank
AF374183). This species is close to the base of the
Stegodyphus genus (J. Johannesen, in prep.). Relationships between S. dumicola and S. tentoriicola
mtDNA haplotypes were analysed using PAUP 4.08b
for the Macintosh (Swofford, 1999). Trees were constructed applying the neighbour-joining method using
the Tamura–Nei distance model (TN), and by
Maximum Parsimony analysis (MP). The TN tested
the model with the highest likelihood ratio, -lnL = 1139
(gamma distribution of rate heterogeneity, a = 0.40)
(MODELTEST 3.04, Posada & Crandall, 1998). In the
MP analysis, all characters were weighted equally and
gaps were treated as a fifth base. In both analyses,
haplotype relationships were analysed with a heuristic search. Strict consensus trees (MP and TN)
were based on bootstrap search (1000 replicates).
Branch-swapping was computed with the treebisection-reconnection algorithm.
RESULTS
We found 15 S. dumicola haplotypes (Table 1) divided
into four lineages. The number of substitutions
between lineages ranged from 12 to 29. Within-lineage
© 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 76, 591–600
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J. JOHANNESEN ET AL.
Table 1. Geographical and colony distribution of S. dumicola haplotypes belonging to four lineages. Colony size was estimated by counting individuals. n.e. = not estimated, N = the number of spiders investigated per colony (females are given
in brackets). Haplotype genealogies are shown in Fig. 4
Colony size
Haplotype
Area
Colony
M
F
N
Outjo
J
K
L
M
39
15
15
7
n.e.
n.e.
n.e.
13
7
6
6
5
A
5
20
4
B
C
I
3
9
7
15
112
n.e.
5 (2)
6 (3)
6
Gamsberg
Q
3
n.e.
3
Omdraie
D
E
F
G
H
15
10
15
4
15
80
38
58
37
118
6
6
6
5
6
(3)
(3)
(2)
(4)
(3)
S
T
U
V
12
3
35
86
14
7
57
137
5
2
6
7
(3)
(2)
(3)
(4)
W
X
Y
Z
49
5
8
8
176
47
50
60
6
6 (3)
6
6
n.e. n.e.
5 (5)
Daan
Viljong
(Windhoek)
Rehoboth
Uhlenhorst
Sesriem
A1
A2
A3
A4
A5
5
A6
B1
B2
B3
B4
B5
C1
C2
D1
D2
2
6
6
5
4
5
6
6
3
differences amounted to between one and five substitutions. Substitutions were predominately found in
the ND1 region, giving for ND1 an among-lineage substitution rate (uncorrected proportional differences)
between 2.65 and 6.00%. The among-lineage substitution rate of 16S ranged between 1.50 and 2.50%
(Table 2).
Generally, colony individuals had the same haplotype (Table 1). We observed an average of 1.13 alleles
per colony. The proportion of polymorphic colonies was
0.13. Haplotype fixation indices showed clearly that
the variance is distributed among colonies, FST = 0.99
(TN); FST = 0.93 (frequency data) (Table 3). These estimates were not inflated by regional fixation of haplotypes (among colonies within localities FSC = 0.98 (TN);
FSC = 0.88 (frequency data)), despite different regional
haplotype distributions (Table 4, see also Table 1).
Simulations indicate that genetic drift in multilineage colonies can not explain lack of mtDNA variation
6
6
6
5
6
5
2
6
3
6
6
6
1
3
6
5
(Figs 2,3). Generally colonies in the field had significantly less within-colony variability than expected
from drift alone. Sampling after five generations produced for all simulations significantly higher variability estimates than observed, all P > 0.001 (not shown
in figures). After 10 generations, only the number of
alleles per colony in colonies with 10 individuals and
two founders did not differ from the observed, number
of alleles = 1.29, P = 0.12. All other simulations were
highly significant, P < 0.0001. After 20 generations,
the number of alleles per colony in colonies with 10
individuals were not different from the observed,
P > 0.25. All other were highly significant, P < 0.001
(Fig. 2)
Sub-samples of six spiders drawn from each simulated category revealed 85–100% (mean: 91%) of the
actual polymorphic colonies. If we assume that 10%
of the polymorphic colonies were wrongly scored as
monomorphic due to sampling just six individuals, the
© 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 76, 591–600
mt DNA VARIATION IN A SOCIAL SPIDER
595
Table 2. Average sequence divergence (uncorrected proportional differences) among four S. dumicola lineages and outgroup species based on 581 characters of a partial mtDNA sequence spanning the genes ND1 and 16S. Below diagonal:
average among lineage ND1 divergence (381 characters). Above diagonal: average among lineage 16S divergence (200 characters). On diagonal in bold: average within-lineage divergence based on total sequence length. For number of mutational
differences within lineages, see Fig. 3
Lineage or species
A1-A6
B1-B5
C1-C2
D1-D2
S. tentoriicola
S. lineatus
A1–A6
B1–B5
C1–C2
D1–D2
S. tentoriicola
S. lineatus
0.004
0.057
0.053
0.049
0.078
0.186
0.023
0.004
0.029
0.040
0.071
0.190
0.025
0.009
0.002
0.035
0.069
0.192
0.020
0.016
0.015
0.003
0.073
0.194
0.030
0.035
0.035
0.030
–
0.188
0.148
0.158
0.157
0.143
0.161
–
Table 3. Mitochondrial DNA differentiation (AMOVA) within and among colonies of S. dumicola
Estimator
Source of variation
df
Variance components
Percentage of variation
Fixation index FST
Tamura-Nei
Among colonies
Within colonies
22
103
9.243
0.029
99.69
0.31
0.997***
Frequency data
Among colonies
Within colonies
22
103
0.427
0.037
92.10
7.89
0.921***
***P < 0.001
0.983***
0.884***
0.815***
0.350***
0.997***
0.925***
***P < 0.001
proportion of polymorphic colonies should be 0.15 not
the observed 0.13. Based on a proportion of 0.15, only
four simulations, all with 10 individuals, were not significantly different from the one observed in the field
(Fig. 3). However, three of these four simulations were
marginally non-significant.
Colonies sampled within 100 m of each other
belonged to the same haplotype lineage, but could be
fixed for different haplotypes – at all localities where
more than one colony was sampled, at least one colony
had a haplotype different from the other colonies.
Two lineages were present at Dan Viljong. Here, the
colonies C and I which each exhibited a private hap-
1.4
1.2
1
40.4
Tamura-Nei
Frequency data
1.6
40.2
40.3
FST
1.8
20.2
20.3
20.4
FCT
2.0
10.3
10.4
FSC
2.2
10.2
Estimators
2.4
Obs
Fixation indices
2.6
Alleles observed per colony
Table 4. Hierarchical analysis of mitochondrial DNA differentiation (AMOVA) among colonies and localities of
S. dumicola; among colonies within localities, FSC; among
localities relative to the total level of sampling, FCT; among
colonies relative to the total level of sampling, FST
Colony size, founders
Figure 2. Average number of alleles per colony after 10
() and 20 () generations as a function of colony size and
number of founders. The observed estimate is given to the
left. Error bars show standard errors. Estimates are based
on subsamples of six randomly drawn individuals per
colony.
lotype belonging to the same lineage, were situated
only 10 m apart. Intra-lineage genealogies indicate a
budding type of haplotype origin, where haplotypes
probably arose from the other area ‘specific’ haplotypes
© 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 76, 591–600
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J. JOHANNESEN ET AL.
Proportion polymorphic colonies
1
10 generations
20 generations
A6
Outjo
A
A1 A2
0.8
0.6
Dan Viljong (Windhoek)
0.4
A3
0.2
Gamsberg
B2
40.2
40.3
40.4
20.2
20.3
20.4
10.2
10.3
10.4
40.2
40.3
40.4
20.2
20.3
20.4
10.2
10.3
10.4
A5
Obs
0
D2
D1
A4
Colony size, founders
C1
C2
Rehoboth B4
Figure 3. Proportion of polymorphic colonies after 10 and
20 generations as a function of colony size and number of
founders. Estimates are based on subsamples of six randomly drawn individuals per colony. Error bars show 95%
confidence intervals based on the proportions of polymorphic colonies from subsets of 20 colonies. The observed proportion is given to the left. The dotted line indicates the
true proportion of polymorphic colonies.
B5
D1
Omdraie
B1
B3
Uhlenhorst
Sesriem
B
D2
23
A1
17
(Fig. 4). For example, haplotype A4, only found at Dan
Viljong, is most related to A3. The same phenomenon
was observed for haplotypes B3 and B4.
The two most polymorphic lineages occurred over
great distances but only one haplotype (B1) was found
at more than one locality. A north–south partitioning
of lineages A and B is observable, with the geographically central lineage D also being phylogenetically
intermediate (Figs 4,5). Basal lineage sequences are
located in central Namibia. Only the basal placement
of lineage A, the most diverged, is ambiguous being
either in central or northern Namibia.
A heuristic analysis of S. dumicola and S. tentoriicola haplotypes resulted in 20 most parsimonious
trees (180, CI = 0.88, RI = 0.88); 50 variable characters were parsimony-informative and 96 were parsimony-uninformative. A consensus tree based on the 20
trees above positioned of S. tentoriicola as outgroup to
the four S. dumicola haplotype lineages. The high
number of trees (20) was caused by recent divergence
at lineage tips. Analysing each lineage for one haplotype (A1, B2, C1, D1) resulted in a single most parsimonious tree (164, CI = 0.92, RI = 0.53); 25 variable
characters were parsimony-informative and 113
were parsimony-uninformative. The TN analysis was
identical to MP in resolution of a common origin of
S. dumicola sequences. The four lineages and outgroup position of the S. tentoriicola sequence was con-
*
C1
A3
B2
11
Figure 4. A, Minimum spanning trees of each of four
S. dumicola haplotype lineages superimposed on their geographical distributions Intra-lineage genealogies indicate a
budding type of haplotype origin, where haplotypes probably arose from the other area ‘specific’ haplotypes. B,
Minimum spanning tree showing connections and number
of mutations between the four lineages. Numbers represent
the number of mutational differences between two connecting sequences with the lowest number of mutations.
The star shows the root placement to S. tentoriicola.
firmed using MP and TN bootstrap analyses (Fig. 5).
Sequence divergence among S. dumicola and S. tentoriicola sequences did not deviate from molecular
clock behaviour, Likelihood-ratio-test statistic delta:
18.53, P > 0.18.
DISCUSSION
This study resulted in two primary findings. First,
and in contrast to our expectations, there was ample
mtDNA variation. Variation was predominately distributed between colonies and each colony was usually
© 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 76, 591–600
mt DNA VARIATION IN A SOCIAL SPIDER
100
83
80
72
A1-A6
100
95
B1-B5
96
86
90
77
100
97
100
96
C1-C2
D1-D2
S. tentoriicola
S. lineatus
Figure 5. Consensus tree for inference of monophyletic
assignment of S. dumicola haplotypes. Bootstrap values
are given for maximum parsimony analysis (upper value)
and Neighbour joining applying the Tamura-Nei genetic
distance (lower value). Intra-lineage haplotypes of S. dumicola have been grouped.
monomorphic. Within localities, colonies with different haplotypes tended to belong to the same haplotype
lineage. Second, S. dumicola haplotypes fell into four
lineages of considerable age. Within at least two of
these lineages, a radiation of haplotypes is occurring.
The geographical distributions of lineages A and B
show that their proliferation is not restricted to one
locality. Therefore, the age of lineages is not only a
consequence of geographical isolation although there
is a tendency for lineages to concur with larger geographical scales. The presence of haplotype lineages
across far distances indicates that colonies are in
constant propagation. Together the above findings
contradict, on a global level, colony coalescence into a
single ‘type spider’ through extreme turnover dynamics. The old age of lineages (equivalent to sequence
divergence) and monophyly of S. dumicola haplotypes
also imply that social behaviour is not a very recent
phenomenon.
COLONY
STRUCTURE
A main implication of the present study is that the
colony structure of S. dumicola leads to female-based
genetic variances. Studies of other species of social
spiders have found division between colony clusters
(Lubin & Crozier, 1985; Roeloffs & Riechert, 1988;
597
Smith & Engel, 1994; Smith & Hagen, 1996). The
novel finding of the current study is that not only
colony clusters but even colonies within colony assemblages may possess discrete genetic (haplotype) differences. Colony discreteness occurs within life-time
dispersal distances. In comparison, Stegodyphus lineatus, a subsocial congener, has an average number of
three haplotypes per population (Laufs, 2001), despite
the fact that S. lineatus shows a pattern of female
dominated population structure and limited matingdispersal within localities (Johannesen & Lubin, 1999,
2001). Thus, S. dumicola has a reduction in the
number of haplotypes converging on a single haplotype per colony. The monomorphic distribution can be
explained neither by genetic drift in colonies originating from multiple founders nor by sampling only six
individuals per colony. In the present study, only three
colonies indicate possible mixing, either at colony
founding or later. However, because the ‘rare’ haplotypes within colonies J and W were found nowhere
else and probably evolved from the ‘common’ colony
haplotype (Table 1, Fig. 4), we cannot distinguish
between mixing and the possibility that the haplotypes arose within those colonies. The only possible
case of intercolony mixing is from colony V (a female).
Probably colony mixing occurs, but single female
colony founding is most important in explaining population structure.
If haplotypes differed within and among neighbouring colonies, they were genealogically similar.
This distribution matches colony founding by single
matri-lineage propagules combined with short-range
dispersal. It resembles, from a female perspective,
‘clonal’ colony propagation and it implies that genetic
processes may be important at both the colony and
individual levels. A colony-level process conforms with
the model constructed by Avilés’ (1993) for explaining
skewed sex-ratios in the social spider Anelosimus
eximius; intercolony (i.e. interdemic) selection and
genetic drift at the colony level are required. The
amount and importance of male-mediated gene flow
still remains to be tested. However, male movement
should not change the female variance pattern
between colonies. Colony founding by single females
or sisters will allow newly mutated haplotypes to
become fixed instantaneously in new colonies, and
could explain the abundant mtDNA variation. The
general colony discreteness of S. dumicola contrasts
that of the diploid eusocial termites in which intracolony mtDNA variation has been found in several
instances (Broughton, 1995; Kaib et al., 1996; Bulmer,
Adams & Traniello, 2001; but see also Thompson &
Hebert, 1998). This is all the more surprising because
termites differ in their breeding system by having only
one or a few reproducing queens. Termite intracolony
variation is evidence of individuals mixing between
© 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 76, 591–600
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J. JOHANNESEN ET AL.
colonies and outbreeding and suggests a different
breeding system than for Stegodyphus.
The phylogeographical pattern of S. dumicola may
even suggest colony propagation as step-wise diffusion
at the total scale of sampling. The basal intralineage
sequences are all found in central Namibia (Fig. 4),
although the basal lineage A sequence is ambiguous.
However, some caution should be exercised in interpreting the geographical pattern because propagule
colony-founding may increase the error of within-area
estimation of variation, as implied at Dan Viljong. We
sampled primarily for differences between neighbour
colonies within localities and may have missed one (or
more) haplotype lineages within a larger local area. In
this sense, there are only seven independent sampling
points to interpret phylogeography.
IS
SOCIALITY IN
STEGODYPHUS
FLEXIBLE?
Regular inbreeding and small family units, typical
for social spiders, have been used to highlight two
very different evolutionary scenarios. Firstly, isolated
groups have been hypothesized to be able to speed up
the evolution of new species. This mode of founderbased speciation emphasizes increasing the genetic
variance between populations. This may lead to
genomic rearrangements and genetic isolation and
increase the probability of novel, advantageous gene
combinations (Templeton, 1980; Goodnight, 1995). In
contrast, small, inbred population units may suffer
from lack of genetic variation and this will reduce
adaptability in ecological time. It is in this latter
context that social spiders have largely been discussed
(but see also Smith, 1986), but which of the above
two scenarios apply for Stegodyphus remains to be
analysed in detail. Wickler & Seibt (1993) found
negative side-effects accumulating with group size in
social Stegodyphus. They speculated that social Stegodyphus establish themselves as eco-species and die
off after a certain time. Hence sociality in Stegodyphus
may be an evolutionary blind alley. Further extinction
probability may come from colony turnover dynamics
and the inbreeding nature of colony living (Avilés,
1997). However, the sequence divergence within
S. dumicola shows that sociality probably has been
present over a long period of time. Divergence within
S. dumicola is equivalent to divergence rates found
between species and isolated cave populations of the
strict troglydont genus Nesticus (ND1: 1.3–7.8%,
Hedin, 1997) but much lower for cryptic species of the
trapdoor spider Aptotichus simus (16S: 6–12%, Bond
et al., 2001). Interestingly, the old age of sociality
is also apparent in the social species Stegodyphus
mimosarum where 35 substitutions separate South
African from Madagascan specimens (J. Johannesen,
unpubl.).
Sociality is considered to be a derived state. The
genus Stegodyphus contains 17 species of which three
species are social; each social species has been classified to a separate species-group (Kraus & Kraus,
1988). Preliminary mtDNA data support three social
groups of ancient origin (J. Johannesen, unpubl.).
In comparison, sociality in naked mole-rat species is
likely to be monophyletic in origin (Faulkes et al.,
1997b). Naked mole-rats were assumed to be highly
inbred (Reeve et al., 1990; Faulkes et al., 1997a),
thus prone to similar colony dynamics as social
Stegodyphus, but recent findings suggest that outbreeding may be common (O’Riain, Jarvis & Faulkes,
1996; Braude, 2000; Ciszek, 2000). Considering
the divergence of haplotypes and variation among
S. dumicola (and S. mimosarum) colonies it is tempting to ask whether sociality necessarily is derived
within the genus Stegodyphus and whether social
species can revert to solitary life (see Henschel,
1991/1992). If sociality is ecologically unstable one
would expect short sequence divergence and lineage
sorting with sympatric subsocial congeners. The
observation that S. dumicola and its nearest
relative S. tentoriicola occur sympatrically (Seibt &
Wickler, 1988) and are genetically distinct suggests
(but does not confirm) a single origin of S. dumicola
rather than multiple origins from a predecessor with
limited gene flow. To clarify lineage sorting (also with
respect to S. tentoriicola, which was collected in South
Africa) sampling over the entire species range of
S. dumicola and of sister species is essential. A test
for evolutionary flexibility of Stegodyphus should be
coupled with an analysis of the intraspecific age of
all social species.
ACKNOWLEDGEMENTS
We thank Jörg Roos, Yael Lubin, Joh Henschel for help
collecting spiders. Special thanks also to Joh Henschel
for organizing logistic support in Namibia. We thank
Dagmar Klebsch for helping in the lab and the Paperclub for discussion. Sampling permission was granted
by the Ministry of Environment and Tourism, Namibia.
This paper was partly financed by a DFG grant (no.
Schn-562/2–2) to J.M.S.
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