Molecular Ecology (2008) 17, 2566–2580
doi: 10.1111/j.1365-294X.2008.03772.x
INVITED REVIEW
Blackwell Publishing Ltd
Multiple paternity in reptiles: patterns and processes
T O B I A S U L L E R *† and M AT S O L S S O N †
*Edward Grey Institute, Department of Zoology, University of Oxford, Oxford OX1 3PS, UK, †School of Biological Sciences,
University of Wollongong, Wollongong, NSW 2522, Australia
Abstract
The evolution of female promiscuity poses an intriguing problem as benefits of mating
with multiple males often have to arise via indirect, genetic, effects. Studies on birds have
documented that multiple paternity is common in natural populations but strong evidence
for selection via female benefits is lacking. In an attempt to evaluate the evidence more
broadly, we review studies of multiple paternity in natural populations of all major groups
of nonavian reptiles. Multiple paternity has been documented in all species investigated so
far and commonly exists in over 50% of clutches, with particularly high levels in snakes and
lizards. Marine turtles and lizards with prolonged pair-bonding have relatively low levels
of multiple paternity but levels are nevertheless higher than in many vertebrates with parental
care. There is no evidence that high levels of polyandry are driven by direct benefits to females
and the evidence that multiple paternity arises from indirect genetic benefits is weak. Instead,
we argue that the most parsimonious explanation for patterns of multiple paternity is that
it represents the combined effect of mate-encounter frequency and conflict over mating rates
between males and females driven by large male benefits and relatively small female costs,
with only weak selection via indirect benefits. A crucial step for researchers is to move from
correlative approaches to experimental tests of assumptions and predictions of theory under
natural settings, using a combination of molecular techniques and behavioural observations.
Keywords: cryptic female choice, multiple mating, multiple paternity, postcopulatory sexual selection,
reptiles, sperm competition
Received 23 December 2007; revision accepted 12 March 2008
Introduction
Sexual selection theory predicts strong selection for traits
that increase reproductive success in both sexes. In males,
mate acquisition is frequently the most severe limitation
on reproductive success and, consequently, male strategies
to ensure mating with multiple females are common and
widespread in virtually all taxa (Andersson 1994; Birkhead
& Møller 1998). In contrast, female reproductive output in
terms of the number of offspring is commonly not limited
by the number of partners and selection on multiple mating
in females should therefore be substantially weaker than in
males (Bateman 1948; Andersson 1994). Research on mating
strategies in the wild has been hampered by the notorious
difficulty with which mating can be reliably observed in
natural populations. However, use of molecular techniques
Correspondence: Tobias Uller, Fax: +44-1865-271168; E-mail:
[email protected]
for paternity assignment has shown that multiple paternity
(and hence multiple mating) by both males and females
are common in natural populations of vertebrates (birds:
reviewed by Griffith et al. 2002; Westneat & Stewart 2003;
mammals: Kitchen et al. 2006; Gottelli et al. 2007; fish:
reviewed by Avise et al. 2002; reptiles: Pearse et al. 2002;
Laloi et al. 2004; amphibians: Laurila & Seppä 1998; Adams
et al. 2005; social hymenoptera: Crozier & Fjerdingstad
2001; data for solitary invertebrates in natural populations
is scarce; Simmons 2001; Simmons et al. 2007).
The link between multiple mating and within-clutch
multiple paternity is not straightforward, however (Dunn
& Lifjeld 1994; Griffith 2007). For example, under selective
fertilization (cryptic female choice; Eberhard 1996) multiple
mating does not necessarily lead to multiple paternity and
clutch sizes necessarily limits the extent to which multiple
mating is reflected by multiple paternity. Thus, categorizing
female mating strategies (e.g. monandry vs. polyandry)
solely upon patterns of paternity (e.g. Richard et al. 2005;
© 2008 The Authors
Journal compilation © 2008 Blackwell Publishing Ltd
M U LT I P L E PAT E R N I T Y I N N AT U R A L P O P U L AT I O N S 2567
Eizaguirre et al. 2007) confuses patterns with processes and
may lead to erroneous conclusions. Furthermore, there is
often a discrepancy between the weight of field and laboratory evidence for multiple mating (Sakaluk et al. 2002). For
example, whereas there is a huge amount of literature on
multiple mating and sexual selection from laboratory experiments in insects, documentation of rates of multiple paternity
(or mating) in natural populations of insects remain comparatively rare and most studies in wild populations have
been conducted on birds (reviewed in Griffith et al. 2002).
Nevertheless, a broad taxonomic approach is required to
tackle the complexities of female mating strategies and
multiple paternity in the wild as any taxon will exhibit
specific shared characteristics that may make one or
more explanations particularly likely or tractable. Birds, for
example, are atypical vertebrates with respect to breeding
(e.g. widespread biparental care) and reproductive traits
[e.g. often lack of an intromittent organ and sequential
(allochronic) ovulation of eggs], which could influence both
selective processes on multiple mating and the degree to
which it leads to multiple paternity. Thus, addressing the
patterns and processes of multiple paternity in natural
populations in a variety of organisms may lead to insights
that are hidden from a specific taxonomic perspective. Here
we conduct the first comprehensive review of the patterns
of multiple paternity in wild nonavian reptiles, a diverse
group of vertebrates, and a critical overview of the underlying processes in an attempt to provide a current consensus
and framework for future research.
A brief overview of reptilian biology
Reptilia (excluding birds) is a diverse group of ectotherm
animals comprising tuataras, crocodilians, turtles and
squamates (lizards and snakes) (see Hedges & Polin 1999
and Townsend et al. 2004 for phylogenies). The extraordinary
diversity in reproductive traits exhibited by reptiles makes
it very difficult to generalize even within well defined
taxonomic groups such as snakes. However, parental care
of hatchlings is absent or rudimentary in all species and
males do not provide any direct resources to the female
before, during or after mating (although they may provide
indirect resources via territory quality). Mating systems are
generally categorized by intense male–male competition
for females and, in many species, female- or resource-defence
polygyny (e.g. Stamps 1977; Martins 1994; Shine 2003).
Reproductive intervals range from days and weeks to years
within lizards and freshwater turtles (e.g. Cogger 1978;
Pearse & Avise 2001), whereas they are more consistently
long (≥ 1 year) in snakes, marine turtles and crocodilians
(e.g. Licht 1984; Seigel & Ford 1987). Breeding normally
occurs according to a seasonal pattern even in tropical
species (e.g. James & Shine 1985; Seigel & Ford 1987) but
sperm production, mating and egg production can be
© 2008 The Authors
Journal compilation © 2008 Blackwell Publishing Ltd
decoupled in time (Seigel & Ford 1987; Aldridge & Duvall
2002). Clutch size is extremely variable, ranging from one
to over 50 in squamates (Fitch 1970), whereas turtles and
crocodilians can lay over 100 eggs in a single clutch (e.g.
Greer 1975).
Causes of multiple paternity in reptile populations: the
role of sperm storage
Multiple paternity can arise via two routes: mating with
more than one male during the same reproductive cycle, or
mating with one or more males during each reproductive
cycle coupled with sperm storage across reproductive cycles.
Sperm storage is widespread in all major reptilian taxa
(reviewed in Schuett 1992; Olsson & Madsen 1998; Sever &
Hamlett 2002; Uller et al. forthcoming). Its evolutionary
causes are debated, however. In some species, low population
densities could lead to a low rate of mate encounter and
therefore a risk of sperm depletion, which would tend to
favour prolonged sperm storage (Gist & Congdon 1998).
This hypothesis is not strongly supported, however, because
mate-encounter rates should be high for many species with
capacity for sperm storage (for example, population densities
of both lizards and snakes are often extraordinarily high, in
particular during the mating season). In this latter category,
selection for cryptic female choice could have driven the
evolution of sperm storage if it enables female control of
paternity and the retention of ‘optimal’ sperm across reproductive cycles (Olsson & Madsen 1998). However, even in
reptiles with prolonged storage of sperm, sperm storage
organs are relatively undifferentiated (Sever & Hamlett
2002) compared to, for example, the case in insects (e.g.
Pitnick et al. 1999). This may suggest that the main reason
for retention and survival of sperm in species where sperm
storage is not obligate (as would be the case when mating
occurs only in autumn and fertilization only in spring;
Schuett 1992; Aldridge & Duvall 2002) can be explained
by a strong selection for sperm longevity resulting from
sperm competition and a quick turnover of reproductive
cycles in females, with only weak selection on sperm storage
in females.
Sperm stored over a long period of time is known to be
capable of fertilizing eggs (e.g. Cuellar 1966; Pearse et al.
2002; Olsson et al. 2007) and multiple paternity resulting from
mixing of stored sperm from matings in previous years
and recently inseminated sperm has been documented in
captive snakes (Agkistrodon contortrix; Schuett & Gillingham
1986) and painted turtles (Chrysemys picta, Pearse et al. 2001).
However, although sperm storage may strongly affect the
pattern of multiple paternity and compromise inferences
about multiple mating (i.e. bias estimates upwards or downwards), its importance is difficult to evaluate due to the
lack of studies. We will return to this issue when discussing
the processes behind the documented patterns below.
2568 T. U L L E R and M . O L S S O N
Patterns of multiple paternity
Estimates of levels of multiple paternity in clutches from
female reptiles in natural populations (and semi-natural
enclosures) are summarized in Table 1 (see Appendix 1 for
methods and statistical analyses). All else equal, the degree
of multiple paternity across species should be positively
correlated with the probability of mate encounters. Although
it is difficult, and potentially misleading to generalize
across species, species with low population densities during
the reproductive season (e.g. sea turtles) and species with
strong pair-bonding (social monogamy; Bull 2000; Chapple
2003) should have lower mate encounters during the female
receptive phase than other reptiles. These two predictions
seem to be upheld: (i) studies of turtles generally show lower
estimates of multiple paternity than studies of squamates
(turtles: 0.42 ± 0.070, N = 22; squamates: 0.55 ± 0.044, N = 35;
χ2 = 6.22, P = 0.013, N = 57; using only the largest data set per
species: turtles: 0.42 ± 0.081, N = 11; squamates: 0.52 ± 0.056,
N = 24; χ2 = 3.82, P = 0.05, N = 35); and (ii) lizards of the
closely related genera Egernia, Oligosoma and Tiliqua generally
show lower levels of multiple paternity than other squamates
(0.21 ± 0.061 vs. 0.61 ± 0.042; χ2 = 20.38, P < 0.001, N = 35;
using only the largest data set per species: 0.23 ± 0.071 vs.
0.59 ± 0.058; χ2 = 10.22, P = 0.001, N = 24). Although these
patterns presumably reflect comparatively low mate encounter and an unusually high degree of social structure
(pair formation; Bull 2000; Chapple 2003; Chapple & Keogh
2006), respectively, the limited phylogenetic distribution
of these traits among species for which we have available
data precludes any further phylogenetically controlled test
of the hypotheses.
The low levels of multiple paternity in social skinks
notwithstanding, multiple paternity in squamates is extraordinarily common, often occurring at levels far above
50% of clutches in natural populations (Table 1). Despite
the caveats regarding presence of sperm storage, this suggests a high degree of multiple mating with different males
during each ovarian cycle by female lizards and snakes
of virtually all species studied to date. In many species of
squamates, the receptivity period is short and a high incidence of multiple paternity should reflect a high mate
encounter, either generated by high population densities or
by active female strategies to ensure multiple mating.
A further caveat is that multiple paternity will more
easily be detected in large, compared to small clutches, both
at the intra- and interspecific levels. In the overall data set,
there was a positive correlation between the average clutch
size and multiple paternity in squamates, but this was mainly
driven by the small clutch size for pair-bonding skinks
[testudines: r = –0.02, P = 0.95, N = 16; Squamates: r = 0.44,
P = 0.023, N = 26; Squamates excluding Egernia and Tiliqua
(clutch size estimates missing for Oligosoma, Table 1): r = 0.31,
P = 0.16, N = 22]. The same pattern was found when we
Fig. 1 Correlation between clutch size (based on sampled eggs)
and the proportion of clutches with multiple paternity in squamates
and testudines. Means per species were used when more than one
estimate was available.
used the mean value per species from all studies (testudines:
r = 0.67, P = 0.070, N = 8; squamates: r = 0.48, P = 0.043,
N = 18; Squamates excluding Egernia and Tiliqua: r = 0.37,
P = 0.20, N = 14; Fig. 1).
Mate encounter may also be affected by the mating system.
In particular, strong territoriality will tend to reduce the
number of males that females will encounter during receptivity. Indeed, the two species of lizards with comparatively
low levels of multiple paternity in natural populations
(Ctenophorus pictus and C. ornatus) are both highly territorial
(and closely related). However, New World territorial
iguanids (Sceloporus virgatus and Uta stansburiana) show a
high frequency of clutches with multiple paternity as do the
territorial wall lizard (Podarcis muralis) (Table 1).
Processes underlying multiple paternity
Direct benefits
Multiple mating, and therefore multiple paternity, can arise
for a number of reasons, some of which are adaptive to
females, some of which are not (see Arnqvist & Nilsson
2000; Jennions & Petrie 2000; Birkhead & Pizzari 2002;
Simmons 2005 for succinct reviews). Benefits are often
divided into two categories—direct and indirect benefits—
that broadly correspond to benefits arising from paternal
contributions to egg production or parental care and those
arising from increased genetic quality, complementarity or
variation (genetic bet-hedging) of the offspring. Most direct
benefits are unlikely to play an important role in reptiles
for two reasons: (i) there is virtually no paternal care among
reptiles (but see Shine 1988 for rare exceptions), which
renders such explanations unlikely; and (ii) there is no
evidence that ejaculates are utilized as resources and, even
if they were, ejaculate sizes are unlikely to be large enough
© 2008 The Authors
Journal compilation © 2008 Blackwell Publishing Ltd
© 2008 The Authors
Journal compilation © 2008 Blackwell Publishing Ltd
Table 1 Multiple paternity in wild reptiles. Studies based on free-ranging animals in outdoor enclosures are indicated with*
Species
No. of clutches examined
% multiple paternity
Clutch size†
Marker
Reference
16
18.8% (3/16)
7.5 (9.3)
Microsatellites
Moore et al. in press
Crocodilians
Am. alligator, Alligator mississippiensis
22
31.8% (7/22)
29.2 (38.0)
Microsatellites
Davis et al. 2001
3
—
70
20
22
3
18
18
23
113
215
3
10
20
17
4
10
13
13
26
2
20
12
7
15
11
33% (1/3)
33%
31.4% (22/70)
95% (19/20)
9.1% (2/22)
100% (3/3)
61% (11/18)
50% (9/18)
4% (1/24)
13.2% (15/113)
33% (71/215)§
66% (2/3)
50% (5/10)
10% (2/20)
0% (0/17)
0% (0/4)
20% (2/10)
92% (12/13)
30% (4/13)
57.7% (15/26)
100% (2/2)
10% (2/20)
50% (6/12)
28.6% (2/7)
20% (3/15)
27.3% (3/11)
20.7 (—)
— (—)
9.8 (—)
28.6 (121.2)
41.3 (—)
15 (—)
38.9 (—)
— (—)
— (—)
5.5 (—)
5.6 (10.9)
12 (—)
— (—)
19.5 (19.5)
— (—)
— (—)
70.3 (117.9)
22.1 (100.8)
22.6 (99.5)
5.2 (—)
32.5 (—)
6.9 (—)
— (—)
7.6 (7.6)
— (—)
2.5 (—)
Microsatellites
Allozymes
Microsatellites
Microsatellites
Microsatellites
Microsatellites
Microsatellites
Minisatellites
Microsatellites
Microsatellites
Microsatellites
DNA fingerprinting
DNA fingerprinting
Microsatellites
Microsatellites
Microsatellites
Microsatellites
Microsatellites
Microsatellites
Microsatellites
Microsatellites
Microsatellites
Allozymes
Microsatellites
Microsatellites
Microsatellites
Bollmer et al. 1999‡
Harry & Briscoe 1988
Moore & Ball 2002
Zbinden et al. 2007
Fitzsimmons 1998
Ireland et al. 2003
Lee & Hays 2004
Peare & Parker 1996
McTaggert 2000‡
Pearse et al. 2001
Pearse et al. 2002
Galbraith et al. 1993
Gailbraith 1993
Crim et al. 2002
Dutton et al. 2000‡
Rieder et al. 1998‡
Hoekert et al. 2002
Jensen et al. 2006
Jensen et al. 2006
Kichler et al. 1999
Valenzuela 2000
Roques et al. 2006
Palmer et al. 1998
Moon et al. 2006
Roqous et al. 2004
Johnston et al. 2006
50
72
16
38
17
8
16
15
17
11
21
33
11.6% (6/50)
23.6% (17/72)¶
25% (4/16)
2.6% (1/38)
64.7% (11/17)
75% (6/8)
93.8% (15/16)
46.7% (7/15)
53% (9/17)
27% (3/11)
19% (4/21)
48.5% (16/33)
— (2.5)
2.0 (2.0)
4.6 (4.2)
3.4 (3.4)
3.2 (3.2)
2.3 (2.3)
— (1.8)‡‡
— (—)
— (3.2)
2.6 (2.6)
2.0 (2.0)
— (5.7)¶¶
Microsatellites
Microsatellites
Microsatellites
Microsatellites
Microsatellites
AFLP
Microsatellites
Microsatellites
Microsatellites
Microsatellites
Microsatellites
Microsatellites
Chapple & Keogh 2005
G. While unpublished data
Gardner et al. 2000, 2002
Stow & Sunnucks 2004
Morrison et al. 2002
Olsson et al. 2005c
E. Wapstra unpublished data
Berry 2006
Stapley et al. 2003
Stapley & Keogh 2006
Bull et al. 1998
Salvador et al. in press
Testudines
Loggerhead turtle, Caretta caretta
Loggerhead turtle, Caretta caretta
Loggerhead turtle, Caretta caretta
Loggerhead turtle, Caretta caretta
Green turtle, Chelonia mydas
Green turtle, Chelonia mydas
Green turtle, Chelonia mydas
Green turtle, Chelonia mydas
Painted turtle, Chrysemys picta
Painted turtle, Chrysemys picta
Painted turtle, Chrysemys picta
Snapping turtle, Chelydra serpentina
Wood turtle, Clemmys insculpta
Leatherback turtle, Dermochelys coriacea
Leatherback turtle, Dermochelys coriacea
Leatherback turtle, Dermochelys coriacea
Olive ridley sea turtle, Lepidochelys olivacea
Olive ridley sea turtle, Lepidochelys olivacea
Olive ridley sea turtle, Lepidochelys olivacea
Kemp’s ridley sea turtle, Lepidochelys kempi
Side-necked turtle, Podocnemis expansa
Freshwater pond turtle, Emys orbicularis
Desert tortoise, Gopherus agassizii*
Gopher tortoise, Gupterus polyptemus
Spur-thighed tortoise, Testudo graeca
Asian tortoise, Testudo horsfieldii*
Lizards
White’s skink, Egernia whitii
White’s skink, Egernia whitii
Spiny-tailed skink, Egernia stokesii
Cunningham’s skink, Egernia cunninghami††
Southern water skink, Eulamprus heatwolei
Southern snow skink, Niveoscincus microlepidotus
Spotted snow skink, Niveoscincus ocellatus
Grand skink, Oligosoma grande††
Mt log skink, Pseudomoia eurecateuixii‡‡
Mt log skink, Pseudomoia eurecateuixii§§*
Sleepy lizard, Tiliqua rugosa
Spanish rock lizard, Iberolacerta cyreni
M U LT I P L E PAT E R N I T Y I N N AT U R A L P O P U L AT I O N S 2569
Tuatara
Tuatara, Sphenodon punctatus*
Species
No. of clutches examined
% multiple paternity
Clutch size†
Marker
Reference
© 2008 The Authors
Journal compilation © 2008 Blackwell Publishing Ltd
Common lizard, Lacerta vivipara
Common lizard, Lacerta vivipara
Common lizard, Lacerta vivipara
Common lizard, Lacerta vivipara
Common lizard, Lacerta vivipara
Common lizard, Lacerta vivipara†††*
Common lizard, Lacerta vivipara‡‡‡*
Sand lizard, Lacerta agilis
Common wall lizard, Podarcis muralis
Ameiva exsul*
Jacky lizards, Amphibolurus muricatus*
Ornate dragon, Ctenophorus ornatus
Painted dragon, Ctenophorus pictus
Striped plateau lizard, Sceloporus virgatus
Side-blotched lizard, Uta stansburiana
51
38
26
44
14
104
22
5
31
11
67
20
51
13
123
47.0% (24/51)
55.3% (21/38)
65.4% (17/26)
68.2% (30/44)
50.0% (7/14)
69.2% (72/104)
72.7% (16/22)
80% (4/5)
87.1% (27/31)
9.1% (1/11)
30.0% (20/67)
25% (5/20)
17.6% (9/51)
61.5% (8/13)
72.4% (89/123)§§§
— (—)
— (—)
— (—)
5.7 (5.7)
5.6 (5.6)
6.4 (6.4)
3.4 (3.4)
— (—)
2.8 (—)
— (3.36)
3.8 (4.2)
2.1 (2.5)
3.6 (3.6)
7.3 (7.8)
2.5 (3.5)
Microsatellites
Microsatellites
Microsatellites
Microsatellites
Microsatellites
Microsatellites
Microsatellites
DNA fingerprinting
Microsatellites
DNA fingerprinting
Microsatellites
Microsatellites
Microsatellites
DNA fingerprinting
Microsatellites
Eizaguirre et al. 2007
Eizaguirre et al. 2007
Hofmann & Henle 2006
Laloi et al. 2004
Laloi et al. 2004
Fitze et al. 2005
Fitze et al. 2005
Gullberg et al. 1997
Oppliger et al. 2007
Lewis et al. 2000
D. Warner unpublished data
Lebas 2001
Olsson et al. unpublished
Abell 1997
Zamudio & Sinervo 2000
Snakes
Water python, Liasis fuscus
Northern water snake, Nerodia sipedon
Northern water snake, Nerodia sipedon*
Northern water snake, Nerodia sipedon††††
Garter snake, Thamnophis sirtalis
Garter snake, Thamnophis sirtalis
Garter snake, Thamnophis sirtalis
Garter snake, Thamnophis sirtalis
Garter snake, Thamnophis sirtalis
Black ratsnake, Elaphe obsolete
Adder, Vipera berus
Adder, Vipera berus
Adder, Vipera berus
14
14
—
81
16
6
4
8
32
34
12
10
13
85.7% (12/14)
85.7% (12/14)¶¶¶
62.1% (—)
58% (46/81)
37.5% (6/16)
50% (3/6)
100% (4/4)
75% (6/8)
59.1% (13/22)‡‡‡‡
88% (30/34)
16.7% (2/12)
80% (8/10)§§§§
69.2% (9/13)
11.7 (9.4)
22.6 (22.6)
— (15.8)
18.0 (18.0)
8.5 (8.5)
15.5 (15.5)
18.3 (18.3)
7.5 (—)
13.8 (13.8)
13.0 (13.0)
8.9 (8.9)
9.1 (9.1)
6.8 (7.7)
Microsatellites
Allozymes
Microsatellites
Microsatellites
Microsatellites
Microsatellites
Microsatellites
Microsatellites
Allozymes
Microsatellites
DNA fingerprinting
DNA fingerprinting
Microsatellites
Madsen et al. 2005
Barry et al. 1992.
Kissner et al. 2005
Prosser et al. 2002
Garner et al. 2002
Garner & Larsen 2005
King et al. 2001
McCracken et al. 1999
Schwartz et al. 1989
Blouin-Demers et al. 2005
Höggren 1995
Höggren 1995
S. Ursenbacher unpublished data
†Given as ‘mean clutch size of genotyped and analysed individuals (mean clutch size at oviposition/parturition).
‡Cited in Pearse & Avise 2001.
§A more conservative, but less likely, measure is 10.7% (23/215).
¶Combined data across three years. Incidence of multiple paternity each year was 16, 17 and 30%.
††Assessed from juveniles in family groups, not hatchlings.
‡‡Only clutches where at least two offspring were assigned paternity included in multiple paternity analyses.
§§Clutches with < 3 offspring explicitly excluded from estimates.
¶¶Hatching success was approximately 38%.
†††Estimates from female-biased population in outdoor enclosures.
‡‡‡Estimates from male-biased population in outdoor enclosures.
§§§Assigning paternity using KINSHIP rather than CERVUS yielded an estimate of 68% (66/97).
¶¶¶A more conservative, but less likely, measure was 57.1% (8/14).
††††Data from two closely situated marshes combined.
‡‡‡‡A more conservative, but less unlikely, measure was 30% (3/10).
§§§§Estimate refers to snakes collected from three different localities, two mainland and one island populations, in south-western Sweden.
2570 T. U L L E R and M . O L S S O N
Table 1 Continued
M U LT I P L E PAT E R N I T Y I N N AT U R A L P O P U L AT I O N S 2571
to significantly contribute to female resource levels (Olsson
& Madsen 1998), in particular since many reptiles tend to
rely heavily on stored resources for reproduction (i.e. they
are commonly ‘capital’ rather than ‘income’ breeders;
Bonnet et al. 1998).
However, a third group of benefits can also be classified as
direct, i.e. ensuring the presence of sufficient sperm numbers
to allow fertilization of eggs. Sperm limitation can arise if
some males are infertile (e.g. due to a lack of mature sperm,
Olsson & Madsen 1996; Olsson & Madsen 1998; Roig et al.
2000) or if some copulations result in transfer of insufficient
sperm numbers (Ridley 1988; Török et al. 2003). The degree
to which multiple mating in female reptiles ensures fertilization success has not yet been systematically addressed.
However, the number of matings (with the same or different
males) was negatively correlated with the incidence of
infertility in the Swedish common lizard (Uller & Olsson
2005) and, in sand lizards, females risk mating with infertile
males if they emerge from hibernation before maturation of
spermatozoa is complete (Olsson & Madsen 1996; see also
Olsson & Shine 1997). Furthermore, evidence from turtles
suggests that sperm storage ensures access to sperm for
production of successive clutches when mate-encounter
rates are low (Pearse & Avise 2001), suggesting that sperm
limitation could be a real problem for females in natural
populations of some reptiles. A potential additional consequence of risk of sperm limitation is that females should
mate with all available males, thereby reducing selection
for precopulatory mate choice.
Indirect benefits
Indirect benefits of multiple mating can arise via at least
four mechanisms that could be relevant for reptiles (Jennions
& Petrie 2000). The most easily grasped is when there is a
second-male fertilization advantage and females mate
multiply to ‘trade up’, i.e. when they meet a male that is of
higher quality than the one(s) they have mated with before
(Halliday 1983; Jennions & Petrie 2000; see Pitcher et al.
2003 for empirical evidence in guppies). The other benefits
arise from an advantage of simultaneous presence of sperm
from multiple males before and during the process of
fertilization. One is by promoting sperm competition among
ejaculates (e.g. Curtsinger 1991; Parker 1998). This will
ensure that eggs are fertilized by sperm from males who
are successful in sperm competition situations and, if this
trait is heritable, their sons will inherit a high competitive
ability under sperm competition (the sexually selected
sperm hypothesis, Keller & Reeve 1995). Alternatively, success
under sperm competition may be (genetically) correlated
with genetic quality more generally (i.e. promoting sperm
competition increases the chances of good genes to the
offspring; Jennions & Petrie 2000; see also Sheldon 1994).
The third mechanism is that multiple mating allows cryptic
© 2008 The Authors
Journal compilation © 2008 Blackwell Publishing Ltd
female choice among ejaculates to increase offspring
genetic quality or complementarity (Zeh & Zeh 1996;
Tregenza & Wedell 2000). The fourth hypothesis is based
on a benefit of multiple paternity per se. Under this
hypothesis, genetic (and presumably phenotypic) diversity
among offspring is favoured because of unpredictable
fluctuations in selective pressures (genetic bet-hedging;
Yasui 1997, 1998, 2001).
We now discuss the relevance of each of these hypotheses
based on patterns of multiple paternity and the biology of
reptiles.
Trading up. The trading up hypothesis predicts that a
female will be more likely to remate if the second (and
third, etc.) male is of higher quality than the previous
male(s). Direct evidence in favour of this hypothesis in
reptiles is lacking although positive correlations between
multiple mating or multiple paternity and hatching
success or offspring viability (Madsen et al. 1992; Olsson
et al. 1994; Blouin-Demers et al. 2005; Eizaguirre et al. 2007;
Zbinden et al. 2007) is consistent with this, as well as some
other hypotheses relating to variation in intrinsic male
quality (see below). However, no studies have shown that
dead, aborted, or otherwise unviable offspring are sired by
particular males, as would be predicted if this was the case.
There is also little evidence that females actively seek
partners, and that different males give rise to offspring of
different phenotypes within a clutch (but see Calsbeek &
Sinervo 2004; Stapley & Keogh 2005). Furthermore, the
only experimental studies to date to investigate female
mating behaviour in relation to mating status and male
quality did not find an increased probability of remating
for females presented with males of higher quality (females
always mated indiscriminately; Olsson et al. 1996; Olsson
2001). The weak evidence for widespread importance of
precopulatory mate choice in reptiles (Tokarz 1995; Olsson
& Madsen 1995) may also make this hypothesis unlikely to
apply in many species. However, the lack of evidence for
mate choice may also reflect a lack of well-designed studies
on female choice in reptiles, in particular with respect to
olfactory cues (e.g. Lopez et al. 2003; Olsson et al. 2004; but
see Jansson et al. 2005). Combining behavioural studies of
mate preferences with molecular assignment of paternity
could provide important insights into the role of the female
in postcopulatory processes.
Promoting sperm competition. The second hypothesis assumes
that males who are good at sperm competition give rise to
offspring (or at least males) that are of high quality (Yasui
1997; Jennions & Petrie 2000). This assumption is untested
in reptiles and its verification would require studies documenting that fertilization success in sperm competition is
a heritable trait or that it is correlated with genetic quality
more generally. No studies of the heritability of fertilization
2572 T. U L L E R and M . O L S S O N
success exist in reptiles and there is also precious little
evidence for intraspecific variation in sperm traits and
their heritability (Schulte-Hostedde & Montgomerie 2006;
Uller et al. forthcoming). However, positive correlations
between number of partners (but not number of fathers)
and offspring viability (e.g. Olsson et al. 1994) are consistent with this theory. It is also worth noting that intralocus
sexual conflict may lead to different fitness returns from
sons and daughters in relation to male sperm competition
success (Pizzari & Birkhead 2002; Arnqvist & Rowe 2005),
which implies that reaping such genetic benefits must
involve sophisticated sex allocation decisions (Pischedda
& Chippindale 2006; Fawcett et al. 2007). This could
involve matching sperm from different males to offspring
sex (Calsbeek & Sinervo 2004) or a more general sex ratio
adjustment at the level of the clutch (Burley 1981; Olsson
et al. 2005a). However, contrary to predictions from the genetic
quality theory, sex ratios are biased towards daughters
when female sand lizards mate with high-quality males
(Olsson et al. 2005a, b; see also Calsbeek & Sinervo 2004
for a potential example of adaptive within-clutch sex ratio
adjustment in U. stansburiana). Thus, it is crucial that the
fitness returns on investment into sons and daughters in
relation to paternal quality is put under empirical scrutiny
rather than simply relying on theoretical model assumptions
(Olsson et al. 2005a, b; Pischedda & Chippindale 2006).
Cryptic female choice. Multiple mating to increase the potential
for cryptic female choice has been championed as the most
likely cause for the evolution of female promiscuity in lizards
(Olsson et al. 1994; reviewed in Olsson & Madsen 1998, 2001).
This idea fits well with the observation that precopulatory
female choice is rare in reptiles (Olsson & Madsen 1995;
Tokarz 1995) and was also supported by early experimental
and fieldwork in sand lizards (Olsson et al. 1996). However,
both this hypothesis, and those relying on ‘good genes’,
suggests that paternity will be strongly skewed towards
one male (Eberhard 1996). Thus, if selection for multiple
mating arises via cryptic female choice or to obtain genetic
benefits via promoting sperm competition, female mating
rate should be consistently higher than the degree of multiple
paternity (i.e. mating is random but fertilization is not).
In fact, multiple paternity in lizards and snakes is extraordinarily common and reach higher levels than that
documented for any other vertebrate group (Table 1) and it
frequently involves more than two males siring offspring
within a given clutch (e.g. 1–5 sires in northern water snakes,
Nerodia sipedon (Prosser et al. 2002); side-blotched lizards,
U. stansburiana (Zamudio & Sinervo 2000); and loggerhead
turtles, Caretta caretta (Zbinden et al. 2007)).
The high level of multiple paternity in the wild hence
represents a problem for the hypothesis of female control
over fertilization. Females may still obtain benefits by mating
multiply if fertilization is random, however, since at least
some offspring would result from fertilizations by highquality (or complementary) males. However, assuming
random mating and that male quality is evenly distributed
(i.e. there is an equal chance of mating with a male being
one standard deviation higher than the mean as with a
male being one standard deviation lower than the mean),
the average fitness of offspring would be the same for singly
and multiply mating females. An alternative explanation
is that there could exist multiple males within a population
that are equally good for a female and that these males
may share paternity whereas males of poorer quality fail
to fertilize any eggs. But with many males of equal quality
present within a given population, selection for cryptic female
choice may not be sufficiently strong to allow mechanisms
to evolve. Clearly, we need experimental tests of the
importance of mating order and individual genotypes
and phenotypes for paternity patterns (Olsson et al. 2004)
before we can accurately address the role of promoting
sperm competition and cryptic female choice in the evolution
of female promiscuity. Ideally, this should be combined
with measures of female fitness in relation to mating frequency and the degree of multiple paternity [both direct
(Fitze et al. 2005; Le Galliard et al. 2005) and indirect via
offspring or embryonic survival (Madsen et al. 1992; Olsson
et al. 1994; Eizaguirre et al. 2007)]. Surprisingly, despite that
the first documentations of a relationship between multiple
mating and female fitness via offspring quality was conducted in snakes and lizards (Madsen et al. 1992; Olsson
et al. 1994), and that one of the species subsequently showed
nonrandom fertilization in mating trials (Olsson et al. 1996,
2004), these studies have not been followed by detailed
laboratory and experimental studies that address model
assumptions and predictions in other squamates. Importantly, at least in many squamates, statistical correction
for mortality during early development (Olsson et al. 1999;
Simmons 2007) can be ensured since resorption of eggs
does not occur (Blackburn 1998; Blackburn et al. 2003) and
all eggs are normally oviposited at the same time, which
generates reliable estimates of embryonic mortality.
Bet-hedging. The fourth indirect benefit of multiple mating
(and paternity) occurs when the creation of genetically
(and phenotypically) diverse offspring within a clutch is
favoured directly, commonly referred to as bet-hedging (Yasui
1997, 1998, 2001). Bet-hedging can evolve under fluctuating
environmental conditions when the optimal phenotype is
difficult to predict at the timing of mating (or fertilization)
since it reduces variance in female reproductive success
(i.e. maximizes geometric mean fitness, Yasui 1998, 2001;
Fox & Rauter 2003; Sarhan & Kokko 2007). Although theoretically plausible, and sometimes referred to as a potential
explanation for high levels of multiple paternity (e.g. Calsbeek
et al. 2007), the conditions that favour genetic bet-hedging
are quite restrictive (Yasui 2001; Sarhan & Kokko 2007).
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Journal compilation © 2008 Blackwell Publishing Ltd
M U LT I P L E PAT E R N I T Y I N N AT U R A L P O P U L AT I O N S 2573
Furthermore, there is little evidence in any taxa that paternal
genotypic variation gives rise to sufficient phenotypic
variation to be of importance under fluctuating selection.
An empirical problem is that a robust test requires a comparison of fitness of females that produce offspring from
multiple fathers with those producing single-fathered clutches
across breeding attempts that reflect the natural variation
in selective regimes. This is clearly a daunting task for any
field based research project regardless of the study organism
and there is currently no available evidence that allow an
evaluation of its importance for reptilian systems (see
Sarhan & Kokko 2007 for a possible example in a butterfly).
Sexual conflict
Multiple paternity can arise without direct or indirect benefits
to females (Lee & Hays 2004; Arnqvist & Kirkpatrick 2005).
Selection on males to mate multiply is uncontroversial and
will be particularly strong in mating systems that lack
paternal care (Andersson 1994). Thus, multiple mating and
multiple paternity will arise whenever the realized mating
system is closer to the male optimum than to the female
optimum. Assuming that there are no direct or indirect
benefits to females from mating with multiple males and
no cost of mating for males (which is doubtful if sperm is
costly, see Olsson et al. 1996), the level of multiple mating in
a population will be set by the frequency of mate encounter
and the costs of mating to females. However, even in the
presence of female costs, males may be able to enforce
copulations. For example, in garter snakes (Thamnophis
sirtalis), males are able to induce cloacal gaping and thereby
allow intromission by pressing the female to the ground
(Shine et al. 2003; Shine & Mason 2005). The level of multiple
paternity will subsequently be affected by processes of sperm
competition, which in the absence of any female-driven
processes might constitute a ‘fair raffle’ (Parker 1998).
Under this scenario, multiple paternity in the wild will
largely reflect the probability of encountering different
males during each reproductive cycle. Importantly, mate
encounter rates are likely to be higher on average in nonterritorial species and species with high population densities
and lower in species that form more stable bonds between
males and females (regardless of whether this is driven
by strong territoriality or other factors). The patterns of
multiple paternity across reptilian taxa are broadly consistent
with this hypothesis. For example, among lizards, pairbonding social skinks show lower degrees of multiple
paternity than does reasonably ecologically similar lacertids
and agamids and, in the latter, some territorial species have
notably low incidence of multiple paternity for squamates
(see Table 1 for references). Furthermore, populations of
olive ridley sea turtles that breed and nest in aggregations
have a higher proportion of multiply sired clutches than
populations with solitary nesting and, across turtle studies,
© 2008 The Authors
Journal compilation © 2008 Blackwell Publishing Ltd
the proportion of multiply sired clutches is positively correlated with breeding population size (Jensen et al. 2006).
However, interspecific patterns should be treated with
caution for a number of reasons:
1 There is insufficient data at present to allow a proper
phylogenetically controlled test of the relationship between
categories, such as pair-bonding, territorial and nonterritorial lizards.
2 The sample sizes for many species are low, suggesting
large confidence intervals. Reassuringly, however, levels
of multiple paternity for some species represented by low
sample sizes have been confirmed with more exhaustive
data (e.g. loggerhead and leatherback turtles, see Table 1
for references).
3 The ecology of many species is simply not sufficiently
well known to allow separation into distinct categories.
For example, the actual opportunities for multiple mating
may not be accurately reflected by male territoriality if
females actively pursue multiple mating, as has been
shown in some birds (e.g. superb fairy wrens; Malurus
cyaneus, Cockburn 2004). Furthermore, although sand
lizards are not territorial, they commonly guard females
after copulation (Olsson et al. 1996; Gullberg et al. 1997),
thereby essentially reducing the probability of female
remating in the same way as would territoriality (but
levels of multiple paternity are still high; Gullberg et al.
1997; Olsson et al. unpublished data).
4 Multiple paternity is not the same as multiple mating.
We have already discussed how indirect benefits to females
can drive biased probability of fertilization (and the
limited evidence thereof) but it is equally true that clutch
sizes and sperm storage may confound the links between
paternity and mating strategies. Although there was
only weak evidence that clutch size explains variation in
multiple paternity among species when pair-bonding
skinks (with low clutch sizes and low rates of multiple
paternity) were excluded, larger females with larger
clutches have higher incidence of multiple paternity in
some species (e.g. Chrysemys picta: Pearse et al. 2002; Lacerta
vivipara: Eizaguirre et al. 2007) and it is uncertain to what
extent this reflects differences in mating strategies.
Furthermore, sperm storage cannot be ruled out as an
important cause of variation among or within species.
For example, in the painted dragon, Ctenophorus pictus,
males mating early in the season (before ovulation of the
first clutch) gain a large proportion of paternity also in
later clutches (Olsson et al. 2007), thereby reducing levels
of multiple paternity both within and across clutches
(Olsson et al. unpublished data). There is also commonly
a substantial variation among populations within the
same species in key predictors, such as population density
(e.g. Pearse et al. 2006), which makes comparison across
species difficult.
2574 T. U L L E R and M . O L S S O N
5 Finally, local and annual variation in climatic conditions
(e.g. temperature, sunshine) will strongly affect reptilian
activity patterns and thereby the strength of pre- and postcopulatory sexual selection (Uller et al. forthcoming), which
may cause variation in multiple paternity at spatial and
temporal scales (Prosser et al. 2002).
The last problem suggests that the preferred approach
to test the role of population parameters on mating and
paternity patterns would be to use experimental manipulation within species, in particular species that show
large variation in key characters in natural populations.
Recent experimental studies of the common lizard, L. vivipara,
have taken important steps towards an understanding of
sexual conflict for mating and paternity patterns. Studies
using experimental enclosures where the adult sex ratio
was manipulated showed that, contrary to predictions, the
proportion of clutches with multiple paternity was not
affected by the availability of males (Fitze et al. 2005; see
also Laloi et al. 2004), but that the incidence of multiple
paternity was not consistent across female age categories
(Richard et al. 2005). Middle-aged females showed the
lowest incidence of multiple paternity (Richard et al. 2005),
which could reflect the outcome of female choice and
sexual conflict. However, the studies also suggested that
male harassment was an important factor in determining
the degree of multiple paternity, since multiple paternity
clutches in male-biased enclosures had more fathers per
clutch on average than multiple paternity clutches in
female-biased enclosures (Fitze et al. 2005). Furthermore,
female reproductive success was reduced in male-biased
enclosures, presumably via increased male harassment
(Fitze et al. 2005; Le Galliard et al. 2005; see also Richard
et al. 2005; Uller & Olsson 2005; Eizaguirre et al. 2007).
However, the lack of data on individual interactions in all
L. vivipara studies (all data comes from paternity analyses)
makes it difficult to evaluate the relative importance of
male and female mating strategies and postcopulatory
processes for the observed patterns of paternity. Thus,
behavioural studies of male and female reproductive
strategies are a necessary and invaluable complement to
molecular methods of paternity assignment (Griffith 2007).
As the studies of L. vivipara and T. sirtalis indicate, the
cost of mating and mate choice may be of critical importance for the evolution of male and female mating strategies
and, consequently, patterns of multiple paternity (see Kotiaho
& Puurtinen 2007). Costs of mating in males are often considered to be negligible (at least in relation to the benefits;
e.g. Bateman 1948; Parker 2006), but studies of the adder,
Vipera berus, suggest that sperm production can infer a
substantial cost (Olsson et al. 1996). Sexually transmitted
disease may also impose an important selective pressure
on the sexual behaviour of both sexes (Boots & Knell 2002;
Knell & Webberley 2004). Unfortunately, our knowledge of
sexually transmitted diseases in wild animals (including
reptiles) remains poor (Knell & Webberley 2004), which
precludes a detailed discussion of its role in the evolution
of mating strategies. Additional costs to female reptiles
include (i) physical and physiological harm; (ii) reduced
time for other activities; and (iii) predation (e.g. Shine et al.
2000, 2003, 2004; Le Galliard et al. 2005). Interestingly, in
L. vivipara, population sex ratios (in semi-natural populations) have a strong effect on female fitness by reducing
female survival and clutch size in male-biased populations
(Fitze et al. 2005; Le Galliard et al. 2005), presumably
because of repeated mating attempts by males that incur both
physical harm (the male bites the female on her abdomen
during copulation and mating is unusually long in L. vivipara,
Bauwens & Verheyen 1985; Heulin 1988), and reduced time
for other activites, such as foraging. This suggests that costs
of mating may be substantial in this species. However,
since females may not necessarily have mated more frequently, or with more males, in male-biased populations,
the costs may simply arise from repeated mating attempts
and female resistance rather than successful matings (Fitze
et al. 2005). Thus, not only mating per se, but resistance to
mating, is an important cost to females that should be
considered both theoretically and empirically.
Concluding remarks
Multiple paternity is ubiquitous in reptiles and occurs at
high levels in all major groups, strongly suggesting high
levels of female promiscuity. Although authors frequently
suggest that indirect benefits to females are the selective
pressure behind multiple mating, the available evidence
suggests that it primarily arises through a combination of
strong selection on male multiple mating (perhaps more so
than in taxa with parental care), low degree of precopulatory
mate choice, high mate-encounter rate and a relatively
moderate cost of repeated mating to females (Lee & Hays
2004). In fact, since the first evidence for indirect genetic
benefits to females via a positive correlation between multiple
mating and offspring viability in the adder, Vipera berus
(Madsen et al. 1992) and the sand lizard, L. agilis (Olsson
et al. 1994, 1996), there has been very little further evidence
to suggest that multiple mating or multiple paternity has
positive fitness consequences in reptiles (but see BlouinDemers et al. 2005; Madsen et al. 2005; Eizaguirre et al. 2007
for correlations between multiple paternity and estimates
of hatching success or offspring viability). Both the sand
lizard and adder studies were conducted on small and
inbred populations. In these populations, multiple mating
with different males resulted in a higher proportion of
viable young (Madsen et al. 1992; Olsson et al. 1994) and,
in the sand lizard, more distantly related males sired the
majority of offspring both in the field and in staged sperm
competition trials (Olsson et al. 1996). However, it is quite
© 2008 The Authors
Journal compilation © 2008 Blackwell Publishing Ltd
M U LT I P L E PAT E R N I T Y I N N AT U R A L P O P U L AT I O N S 2575
possible that a general tendency towards female promiscuity
in these species have evolved in the absence of indirect
female benefits via strong selection on males (as envisioned
above, see also e.g. Shine et al. 2003, 2004) and that benefits
only arise secondarily due to population-specific characters,
such as low genetic variation and high degree of inbreeding
depression (Olsson & Madsen 2001). Indeed, both sand
lizards and adders show high levels of multiple paternity
even within small populations (above 65% for both species;
Gullberg et al. 1997; Ursenbacher et al. unpublished data),
suggesting limited paternity bias in relation to genetic
compatibility in the wild. Overall, there is currently little
evidence that indirect benefits are important selective
forces in reptiles in general and, in fact, the high levels of
multiple paternity may argue against both cryptic female
choice and ‘good genes’ scenarios. Similar conclusions
have recently been advocated for birds (Westneat & Stewart
2003; Arnqvist & Kirkpatrick 2005, 2007; Albrecht et al.
2006; Akçkay & Roughgarden 2007; see also Kotiaho &
Puurtinen 2007). Thus, we suggest that researchers should
avoid relying too heavily on hypothesis of indirect benefits
and take seriously models that make fewer assumptions
and in which ecological parameters such as mate-encounter
rates and costs of mating are of prime interest. Although
they may be less spectacular, and require logistically
challenging behavioural studies, such approaches are
more likely to capture the evolutionary dynamics of mating
strategies and multiple paternity in the wild. Nevertheless,
our conclusion also reflects the paucity of studies that
experimentally test assumptions (e.g. do high-quality males
sire high-quality offspring? what is the cost of mating?)
and predictions (e.g. do females bias fertilization success
according to male quality?) from sexual selection and sperm
competition theory. Many reptiles are well suited for studies
that can bridge the gap between laboratory studies and
fitness estimates in the wild (Wapstra et al. 2007). Given
that the evidence is strong that multiple paternity is prevalent in all reptilian taxa, the time is ripe to move on from
correlative to experimental approaches and to put theoretical
models to the test.
Acknowledgements
We are grateful to Sylvain Ursenbacher, Dan Warner, Erik Wapstra
and Geoff While for providing unpublished data and to Thomas
Madsen, Tom Pizzari, Charlie Cornwallis and one anonymous
reviewer for discussions. T. Uller was supported by the WennerGren Foundations and the Australian Research Council. M. Olsson
was supported by the Australian Research Council.
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2580 T. U L L E R and M . O L S S O N
Appendix 1
Materials and methods for data collection and statistical
analyses
Data were collected using literature searches of the ISI Web
of Science and Biological Abstracts and by screening all
papers initially obtained. Furthermore, we contacted researchers we knew had data and asked them to provide
unpublished results. Information on the mean clutch size
was not always available in the original publication and is
indicated by ‘—’ in Table 1. Statistical analyses were only
conducted on studies in natural populations (i.e. excluding
semi-natural enclosures).
Overall, there was a negative correlation between the
proportion of clutches with multiple paternity and the
(log-transformed) total number of clutches examined for
both major groups for which we had data (testudines:
r = –0.36, P = 0.10, N = 22; squamates: r = –0.38, P = 0.023,
N = 35). This patterned disappeared when using means per
species (testudines: r = –0.44, P = 0.20, N = 10; squamates:
r = –0.16, P = 0.47, N = 23). We conducted three analyses
of the data based on a priori expectations. First, we used
logistic regression (proc genmod, SAS 9.12) with the number
of clutches with multiple paternity as the numerator and
the total number of examined clutches as the denominator,
a binary distribution and a logit link function to test for a
difference between testudines (the vast majority of which
were marine turtles) and squamates. The rationale being
that population densities (and hence mate-encounter rates)
of the former are frequently assumed to be smaller than for
the latter. Second, we used the same approach to test for
a difference between pair bonding squamates (genera
Egernia, Oligosoma, and Tiliqua) and other squamates, based
on the prediction that social monogamy should lead to
lower mate-encounter rates and possibly higher cost of
multiple mating (e.g. via mate desertion; Chapple 2003).
We conducted our analyses twice; both using all data from
natural populations and reducing the data set to one observation per species. In the latter analyses, we consistently
retained the study with the highest sample size. It should
be noted, however, that despite the nonindependent replication of species in the former, the reduced analysis may
actually be more misleading, as some of the species for
which we had multiple estimates deliberately included
populations that differ in population size or density. Consequently, the remaining multiple paternity data in the
reduced data set could become biased towards highdensity populations (since the number of clutches sampled
should be higher). We also conducted correlation analyses
between the proportion of clutches with multiple paternity
and the mean clutch size of paternity-assigned offspring to
evaluate to what extent clutch sizes may constrain paternity estimates at the interspecific level. We did this both
using the full data set and using the average across studies
for species with more than one study.
Because our main predictors show strong phylogenetic
conservatism, the data does not allow a meaningful analysis
using independent contrasts. Thus, all analyses are potentially confounded by phylogeny and some taxa are clearly
over-represented (Table 1) and the results from the statistical
analyses should be considered preliminary and only serve
as a complement to the extensive narrative evaluation
rather than provide conclusive evidence in favour of a specific hypothesis. More detailed quantitative comparative
analyses of covariation between multiple paternity and
traits important in pre- and postcopulatory sexual selection
should await further accumulation of data from natural
populations (see Uller et al. forthcoming for detailed
discussion).
© 2008 The Authors
Journal compilation © 2008 Blackwell Publishing Ltd