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Snake Mating Systems, Behavior, and Evolution: The Revisionary
Implications of Recent Findings
Jesu´s A. Rivas and Gordon M. Burghardt
University of Tennessee, Knoxville
Sexual selection and mating systems profoundly influence the behavior and psychology of animals.
Using their own studies of green anacondas (Eunectes murinus) and reviewing other recent studies, the
authors conclude that incomplete data derived from a few well-studied snake species have led to general
acceptance of polygyny as the dominant mating system in snakes. New data on behavior, paternity, and
life history in a diverse taxonomic array of snakes support the view that polyandry is not only common
in snakes but may have been the ancestral mating system. This interpretation helps to explain many
seemingly paradoxical behavioral differences between lizards and snakes, such as the lack of territorial
systems in most snakes and their frequent female-biased sexual size dimorphism.
Comparative studies are necessary for drawing conclusions on
the role of ecology and evolution in the behavioral and psycho-
logical attributes of animals at different taxonomic levels. How-
ever, for these studies to be most informative, they must include
appropriate samples of taxa evaluated in an unbiased manner.
Recent literature has documented how cultural, sexual, and per-
sonal biases can cloud scientific judgment (Gowaty, 1994, 1997;
Marsh & Hanlon, 2004; Rivas & Burghardt, 2002a; Ruse, 1999).
In this contribution, we suggest that lack of balanced information
about the mating systems of different taxa of snakes, along with
uncritical interpretation of the data at hand, has prejudiced general
conclusions about snake mating behavior and the resulting mating
systems. We discuss recent data and reinterpret earlier findings
that led to the prevalent notion that polygyny is the primary, if not
universal, mating system in snakes. We also briefly discuss the
implications of acceptance of these conclusions for understanding
the evolution and comparative psychology of snakes.
Snakes have been suggested as a prime group for testing eco-
logical and evolutionary hypotheses, including those on mating
systems (Shine & Bonnet, 2000). However, despite the fact that
there are more than 3,000 species of snakes (Greene, 1997), most
of the detailed field and experimental literature dealing with mat-
ing behavior in snakes comes from limited taxonomic groups (e.g.,
natricines) studied in a limited distribution range (North America).
In particular, in the far north of the United States and southern
central Canada, there are large hibernacula of garter snakes
(Thamnophis sirtalis). They emerge in large numbers in spring,
and most mating takes place over several weeks at these sites. This
expedites efficient collection of large data sets on mating behavior.
It leads, however, to two potential problems. The first is that a
disproportionate number of studies have been performed with only
one species, often considered a model for serpent reproductive
behavior and physiology, with a consequent handicapping of ob-
taining the diverse database needed for comparative studies (Ross-
man, Ford, & Seigel, 1996). The other problem is that most of the
research on mating behavior in T. sirtalis has been done in only
one geographic location at the extreme northern limits of the
species’ geographic range, which may not even be representative
of this species’ typical habitat and social environment. In fact,
virtually no other snakes live in these cold climates.
The Status Quo: Polygyny in Snakes
Polygyny is typically represented by species in which a few
males monopolize access to many females or in some way manage
to gain the benefit of matings with multiple females, relegating
most males in the population to bachelorhood. Classic representa-
tive examples would be northern elephant seals (Mirounga an-
gustirostris) or the red deer (Cervus elaphus). In these cases, only
a few males obtain mating, and most of the other males either do
not mate at all or accomplish very few of the matings (Clutton-
Brock, Albon, & Guiness, 1988; Le Boeuf & Reiter, 1988). In
lizards and snakes (Squamata), a heavily documented example of
this typical polygyny is the green iguana (Iguana iguana; Dugan,
1982; Rodda, 1992). The variance in mating success produces
selection pressure for traits that give males a mating advantage in
male–male competition as well as attractiveness to females. These
Jesu´s A. Rivas, Department of Ecology and Evolutionary Biology,
University of Tennessee, Knoxville; Gordon M. Burghardt, Department of
Psychology and Department of Ecology and Evolutionary Biology, Uni-
versity of Tennessee, Knoxville.
We thank the Wildlife Conservation Society, the National Geographic
Society, Zoo de Doue la Fontaine-France, Ministerio del Ambiente, Ven-
ezuela, and the University of Tennessee for financial and logistic support.
We also thank COVEGAN, Estacio´n Biologica Hato El Frı´o, and Agro-
pecuaria Puerto Miranda for help in logistics and for allowing us to work
on their land. We also thank Christine Strussman and Renatta Platenberg
for sharing relevant unpublished data on their study animals. We are
indebted to L. M. Almli, P. T. Andreadis, H. W. Greene, R. G. Shine, and
J. S. Placyk for providing useful editorial comments on the manuscript.
This research is based in part on a doctoral dissertation completed by Jesu´s
A. Rivas at the University of Tennessee, Knoxville.
Correspondence concerning this article should be addressed to Jesús A.
Rivas, Department of Ecology and Evolutionary Biology, University of
Tennessee, Knoxville, TN 37996. E-mail: jesus@anacondas.org
Journal of Comparative Psychology Copyright 2005 by the American Psychological Association
2005, Vol. 119, No. 4, 447– 454 0735-7036/05/$12.00 DOI: 10.1037/0735-7036.119.4.447
447
traits can include overall body size or secondary morphological,
behavioral, or physiological attributes. In snakes, as well as in
other taxa, adult male size relative to adult female size increases in
those species with male–male combat (Shine, 1994). However, as
we discuss below, there is no documented case of a male monop-
olizing access to several females in an equivalent manner to the
cited mammalian or lizard taxa.
The influential Emlen and Oring (1977) framework for under-
standing the diversity of mating systems relies on the degree to
which mates can be monopolized, the spatial distribution of re-
sources (and thus the underlying ecology), and the availability of
mates. Specifically addressing mating systems in snakes, several
authors (Duvall, Arnold, & Schuett, 1992; Duvall, Schuett, &
Arnold, 1993) proposed an alternative quantitative genetic-based
model for the evolution of snake mating systems utilizing the
sexual selection gradient, the regression of number of mates on
fecundity. In this scheme (formally generalized to all animals in
Arnold & Duvall, 1994), sexual selection is greater on the sex that
benefits more from increased matings in terms of number of
offspring. Thus, in polygamy and monogamy, the gradients are
similar for both sexes; in polygyny, greater for males; and in
polyandry, greater for females. On the basis of their understanding
of snake biology, Duvall et al. (1993, p. 171) wrote, “because of
the phylogenetic momentum for polygyny among the snakes,
neither polyandry nor polygamy as defined in fig. 5.2 are likely to
occur.” However, no reference or source was provided for this
statement. Within polygyny, these authors diagrammed and listed
four types that they claimed encompass virtually all snakes: female
defense polygyny (mate guarding), hotspot polygyny, prolonged
mate-searching polygyny, and explosive mating assemblage po-
lygyny. Territorial or resource defense polygyny was mentioned as
a possible, but not yet documented, fifth type. Lek polygyny was
viewed as even less likely in snakes.
In fact, virtually all reports of mating systems of snakes regard
them as polygynous (Duvall et al., 1992, 1993; Duvall & Schuett,
1997; Shine & Fitzgerald, 1995). Recent articles on snake repro-
duction that have reviewed or expanded the evidence of mating
systems in snakes have continued to use polygyny as a framework
to analyze their data (Pearson, Shine, & Williams, 2002; Shine,
Langkilde, & Mason, 2003b). However, the requisite multiple
matings with several females by individual males per breeding
season have been largely assumed (Gibson & Falls, 1975; Schuett,
1982) and seldom documented. Alternatively, a male courting
multiple females has been considered as evidence of multiple
mating by males without confirmation as to whether those court-
ships were successful (Blanchard & Blanchard, 1942; Brown &
Weatherhead, 1999b; Shine & Fitzgerald, 1995; Weatherhead,
Barry, Brown, & Forbes, 1995). Other reports have documented
multiple mating by both males and females (Madsen, Shine, Lo-
man, & Hakansson, 1993) or have lacked supporting evidence that
the males obtained exclusive access to the females (Blouin-
Demers, Gibbs, & Weatherhead, 2005; Duvall & Schuett, 1997;
Madsen, Shine, Loman, & Hakansson, 1992; Prosser, Weather-
head, Gibbs, & Brown, 2002). In short, polygyny requires copu-
lation by a male with several females during the reproductive
season, and such data from the field are sparse (see Table 1).
Furthermore, few studies have shown that multiple matings lead to
males siring offspring in multiple females (Prosser et al., 2002, is
an exception). Thus, despite widespread evidence that females
mate with multiple males and little evidence of multiple mating of
females by males, snake biologist have persisted in viewing mating
systems of snakes as polygynous.
Table 1
Snake Species That Breed in Multiple Breeding Aggregations and Snake Species in Which Multiple Mating by Females or Males in
the Same Year Has Been Documented
Species
Multimale
breeding
aggregation
Multiple
mating in
females
Multiple
mating
in males
Multiple
paternity
confirmed Source(s)
Boa constrictor Y Bertona & Chiaraviglio (2003)
Crotalus viridis viridis Y Duvall & Schuett (1997)
Elaphe obsoleta Y Y Blouin-Demers, Gibbs, & Weatherhead (2005)
Eunectes murinus Y Y Rivas (2000); Rivas & Burghardt (2001b)
Eunectes notaeus Y C. Strussman (personal communication, March 1999)
Laticauda colubrina Y Shetty & Shine (2002)
Morelia spilota Y Pearson, Shine, & Williams (2002); Slip & Shine (1988)
Nerodia sipedon Y Y Brown & Weatherhead (1999a, 1999b)
Nerodia sipedon Y Y Y Barry, Weatherhead, & Philips (1992)
Nerodia sipedon Y Y Y Y Prosser, Weatherhead, Gibbs, & Brown (2002); Weatherhead,
Prosser, Gibbs, & Brown (2002)
Thamnophis butleri Y Y Albright (2001)
Thamnophis sirtalis sirtalis Y Y Gibson & Falls (1975); McCracken, Burghardt, & Houts
(1999); Schwartz, McCracken, & Burghardt (1989)
Thamnophis sirtalis parietalis Y Many sources: e.g.,
Vipera berus Y Y Madsen & Shine (1993c); Madsen, Shine, Loman, &
Hakansson (1992, 1993); Shine, Langkilde, & Mason
(2003a)
Vipera berus YYHo¨ggren & Tegelstro¨m (1995); Stille, Madsen, & Niklasson
(1986)
448
RIVAS AND BURGHARDT
Polygyny Versus Polyandry in Snakes
In a long-term field study, Rivas (2000) described the mating
system of green anacondas (Eunectes murinus) as polyandrous
(see also Rivas & Burghardt, 2001a, 2001b) based on over 45
mating aggregations in an intensively studied population with
hundreds of marked individuals. One female lies on the mud or in
shallow water, and males, up to 13 of them, approach and coil
around her to court and attempt to mate. Such mating aggregations
may last for up to a month, and males that find a female tend to
stay with the same female until the end of her attractive period.
There is no evidence of the males going out to look for other
females after they mate. Although the female mates multiple times,
there is thus no evidence of males mating with more than one
female in a given season. Perhaps this is because the females are
dispersed in the landscape and difficult to find. Rivas’s (1998,
2000) and Rivas and Burghardt’s (2001a, 2001b, 2002b) reports of
polyandry in anacondas are unusual because individual anacondas
were tracked for several years. It is interesting to note that ana-
condas are the first species in which the word polyandry has been
used to describe, and best describes, the mating system observed.
It is, perhaps, not the only or the first instance in which polyandry
has been documented but was previously unrecognized.
Other than the work by Rivas and Burghardt (e.g., Rivas, 2000;
Rivas & Burghardt, 2001b), the closest that some authors have
come to acknowledging polyandry has been by using the word
promiscuity (Shine & Fitzgerald, 1995), but no further discussion
has been provided. Even in that study, all findings were analyzed
in the light of “female defense polygyny” or “mate-searching
polygyny” (Shine & Fitzgerald, 1995, p. 496). The work by
Prosser et al. (2002) is an exception to this trend as they docu-
mented successful multiple mating by females as well as by males.
However, they did not assign any label to characterize the mating
system. We have presented data implicating polyandry in snakes in
recent years at scientific meetings and conferences (Rivas, 1998;
Rivas & Burghardt, 2001a, 2002b) to skeptical audiences. Inter-
estingly enough, some colleagues aware of our arguments have
recently mentioned polyandry when analyzing their work (e.g.,
Blouin-Demers et al., 2005).
We think that virtually all detailed studies of snake reproductive
behavior, viewed objectively, show that snakes’ reproductive bi-
ology is more consistent with polyandry than with polygyny. All
evidence suggests that during reproduction, males spend extensive
time and energy courting and mating. During this period, males
feed rarely or not at all. Also, they often choose to mate with the
females that are more fertile or more likely to breed (see Table 2).
Males searching for and courting females may suffer high mortal-
ity in the wild as a result of their mating investment, which further
raises the cost of courting several females (see Table 2). Male
snakes show assortative mating in which they seek to mate with
the larger, more fertile, or otherwise more attractive females (see
Table 2). Males thus choose females selectively instead of mating
indiscriminately, as would be expected in typical examples of
polygyny, in which males typically do not make a large reproduc-
tive investment per mating. Such male choosiness that conflicts
with multiple mating by male snakes is an important selection
pressure because truly polygynous males should maximize the
number of mates and minimize courtship duration and investment
per mating event.
Table 2
Snake Species Reported With Traits Associated With Polyandry: Male Choice or Large Male Reproductive Investment (Through
Energetic Investment, Forfeiting Feeding for Long Periods of Time, or Suffering Strong Predation Pressure During the Mating
Season)
Species
Choosy
males
Large male
mating investment Source(s)
Arizona elegans Y Aldridge (2001)
Coluber viridis viriflavus Y Bonnet, Naulleau, & Shine (1999)
Crotalus horridus Y O’Leile, Beaupre, & Duvall (1994)
Elaphe longisimus Y Bonnet, Naulleau, & Shine (1999)
Elaphe obsoleta Y Y Blouin-Demers, Gibbs, & Weatherhead (2005)
Eunectes murinus Y Y Rivas (2000); Rivas & Burghardt (2001b)
Eunectes murinus Y Rivas (2001); Rivas & Owens (2000); Rivas, Thorbjarnarson, Owens,
& Mun˜oz (1999)
Laticauda colubrina Y Y Shetty & Shine (2002)
Liasis fuscus Y Madsen & Shine (2000)
Morelia spilota Y Shine & Fitzgerald (1995); Slip & Shine (1988)
Natrix natrix Y Luiselli (1996); Madsen & Shine (1993b)
Nerodia sipedon Y Y Prosser, Weatherhead, Gibbs, & Brown (2002); Weatherhead,
Prosser, Gibbs, & Brown (2002)
Nerodia sipedon Y Brown & Weatherhead (1999a); Weatherhead, Barry, Brown, &
Forbes (1995)
Thamnophis sirtalis parietalis Y Y Shine, LeMaster, Moore, Olsson, & Mason (2001); Shine, O’Connor,
LeMaster, & Mason (2003)
Thamnophis sirtalis parietalis Y Garstka, Camazine, & Crews (1982); Shine, Langkilde, & Mason
(2003a, 2003b); Shine & Mason (2001); Shine, Olsson, Moore,
LeMaster, & Mason (2000); Shine, Phillips, Waye, LeMaster, &
Mason (2003)
Vipera berus Y Madsen, Shine, Loman, & Hakansson (1993)
449
SNAKE MATING BEHAVIOR
The ratio of available females per male, or operational sex ratio
(OSR), is far less than one to one for many snake species (Arnold
& Duvall, 1994, preferred to use the breeding sex ratio, the ratio
of breeding males to females, but the following argument is
similar). Female snakes make very large reproductive investments
and often cannot recuperate rapidly enough to reproduce every
year, leading to male-biased OSR (Bonnet, Naulleau, & Shine,
1999; Madsen & Shine, 1993a; Rivas, 2000; Shine, Langkilde, &
Mason, 2003a, 2003b). A male-biased OSR creates a great poten-
tial for reproductive females to mate multiple times (Barry, Weather-
head, & Philips, 1992) and reduces opportunities for many males.
Finally, the most convincing argument that the dominant mating
system in snakes is not polygyny is the fact that multiple mating
and multiple paternity have been found in all the species in which
they have been studied in detail (see Table 1). Thus, anaconda
polyandry might not be just a rare exception to the Duvall et al.
(1993) model; true polygyny might not be nearly as common in
snakes as currently believed. When that model was developed,
there was not enough empirical evidence to suggest how probable
polyandry may be in snakes, but over the past 10 years, there has
been a substantial increase in the literature dealing with snake
reproductive biology. Currently, it is evident not only that poly-
andry might be more common than formally thought but also that
sensu stricto polygyny (in the sense used for mammals and lizards
cited above; see also Arnold & Duvall, 1994) might not even apply
to snakes.
We should note at this point that our effort is not just about
accepting a word or label, as new ones can become as constraining
as the old, but to use an alternative lens to view and interpret
empirical data. We also feel that within a population, it is possible
for different mating systems to occur, such as in the human
species, which can be typed as monogamous, serially monoga-
mous, or moderately polygynous.
However, the problem with researchers resisting the hypothesis
that the mating system of the snake may not be polygynous goes
beyond the simple issue of terminology to how scientists interpret
and direct their research. For instance, there have been several
studies demonstrating that males obtain mating advantages for
being larger, yet the males in those species are smaller than the
females (Madsen & Shine, 1993c; Shine et al., 2000; Weatherhead
et al., 1995). Sexual selection theory predicts that the sexual
selection gradient is stronger in animals that obtain mating advan-
tages from multiple mating. If the males were polygynous, they
would be under stronger selection pressure (higher sexual selection
gradient) than females because of the benefit of mating with
multiple females (Arnold & Duvall, 1994) and would therefore
grow larger if large size benefited their mating abilities. The
research done by scholars trying to explain why males do not grow
larger than females is a consequence of the mistaken assumption of
polygyny. In a polyandrous system, mating advantage for large
size in males is not expected to produce larger males, as the
sexual selection gradient in males is lower than in females (Arnold
& Duvall, 1994). The abundant literature documenting unsuccess-
ful attempts to explain this apparent dilemma (Brown & Weather-
head, 1999a, 1999b; Madsen & Shine, 1993b; Prosser et al., 2002;
Weatherhead et al., 1995; Weatherhead, Prosser, Gibbs, &
Brown, 2002) suggests that this is more than a simple issue of
terminology.
Evaluating Data on Mating Behavior in Snakes
The secretive nature of many snakes and other difficulties that
snake researchers have had in obtaining valid data on snake mating
behavior have contributed to the poor database available for
snakes. In addition, however, snake researchers may have been
misled by the voluminous sexual selection literature on organisms
that do not grow much after adulthood (mammals, birds, and
insects) and that also may have a size-independent clutch size, thus
overlooking suggestive data that were available. This is, perhaps,
a consequence of most snake biologists being male (Wilson,
1998), which may have biased their interpretations of data. Evi-
dence of this possible bias in interpreting snake mating behavior
can be found in an apparent double standard in documenting
multiple mating. Observations of males courting several females
have been considered as evidence of polygyny, but observations of
a female being courted by several males have not constituted
sufficient grounds to conclude polyandry or even multiple mating
in females. In fact, unequivocal evidence of copulation with mul-
tiple males has not been enough to even suggest that females may
be polyandrous, whereas scant field evidence of multiple mating in
males has been grounds to conclude that they are polygynous.
Although there were scattered reports (Gibson & Falls, 1975;
Schuett & Gillingham, 1986), it was not until DNA and molecular
studies conclusively proved several sires in the litters in the well-
studied common garter snake, Thamnophis sirtalis (Schwartz, Mc-
Cracken, & Burghardt, 1989), that the existence of multiple female
mating and resulting multiple paternity of her offspring was seri-
ously recognized; even that species is still being considered as
polygynous. Since then, studies using molecular methods to assess
paternity have found that multiple paternity is the norm in snakes
across a wide variety of families, whereas molecular data for
“multiple maternity” are singularly lacking in naturalistic studies
(see Table 1). Even in the few documented cases, however, the
word polyandry was seemingly avoided until very recently (see
below). Such biases influencing the interpretation of data have
been documented before in other taxa (Cunningham & Birkhead,
1997; Gowaty, 1994, 1997). As we have argued elsewhere (Rivas
& Burghardt, 2001b, 2002a), such research bias can be reduced
through attempting to take into account the attributes of the species
under study and the way its members perceive and respond to the
world, an approach called critical anthropomorphism (Burghardt,
1985). Nonanthropomorphic and allegedly objective approaches
are not a sufficient safeguard against unwitting and uncritical
anthropomorphism in interpreting data (Rivas & Burghardt,
2002a). However, as pointed out below, misleading comparative
and evolutionary inferences are also involved.
We conclude that given the available evidence, the dominant
mating system in snakes is not polygyny. The most common
mating system in snakes is polygynandry or even polyandry in
some cases. We prefer polygynandry instead of promiscuity be-
cause the latter really means lack of discrimination, and mating
with multiple partners does not necessarily involve lack of dis-
crimination, for several potential partners might meet the desired
standards.
450
RIVAS AND BURGHARDT
Snake Behavior, Size Dimorphism, and Evolution
The origin of snakes continues to be controversial although their
placement as a derived squamate reptile aligned with lizards is
accepted. A recent analysis (Greene & Cundall, 2000) contradicted
the view that snakes originated in a marine environment (Caldwell
& Lee, 1997) and supported early views that snakes as a group
evolved in terrestrial environments (Greene & Cundall, 2000),
probably in a subterranean (fossorial) habitat (Forstner, Davis, &
Are´valo, 1995; Gans, 1975; Lee, 1997; Rieppel, 1988). The con-
strained mobility of these early snakes in a fossorial environment
could account for a lower encounter rate with both mates and prey.
In an aquatic habitat, it would also be harder for snakes to follow
scent trails, and the encounter rate with mates would also be
expected to be low (Shine, 1993). Thus, a low encounter rate with
potential mates seems to be the most likely scenario in the evolu-
tionary history of snakes.
One of the values of comparative studies is the opportunity to
assess which traits are primitive for a clade and which ones are
more derived. In trying to understand the evolution of the mating
system, because squamate reptiles other than serpents have diverse
evolutionary lineages, we focus on the accepted closest extant
saurian relatives of snakes, the Varanoidea (monitors, Varanus,
Lanthanotus; beaded lizards, Heloderma; Forstner et al., 1995;
Lee, 1997; Pianka & Vitt, 2003). There are several traits of snakes
as a group that differ from their sister taxa, that may support or
enhance nonpolygynous systems, and that may be derived from a
low encounter rate. For instance, snakes lack the territoriality and
male-biased sexual size dimorphism (SSD) that are common in
their squamate relatives (Phillips, 1995; Pianka & Vitt, 2003;
Shine, 1994; Stamps, 1983; Wikramanayake & Dryden, 1988).
Territoriality is less marked in Varanoidea than in many other
groups of lizards (although injurious fights occur), but the lack of
territoriality in snakes may also relate to the difficulty they have in
defending feeding or mating sites because their visual and auditory
abilities are often limited, and chemosensory vigilance may be
impractical in the relatively large areas and complex environments
in which many snakes live. Furthermore, typical male–male com-
bat, so common in polygynous vertebrates, has been documented
in only about 6% of all snake species and appears totally lacking
in entire lineages, including the seven most basal families (Schuett,
Gergus, & Kraus, 2001), which leads us to conclude that such
combat is a derived trait in snakes. There are also a few other
important differences between snakes and varanid (or other closely
related) lizards that might be due to the same evolutionary path.
First, snakes tend to make larger relative reproductive investments
than do lizards. Second, snakes very seldom have multiple clutches
or litters in a year (Seigel & Fitch, 1984). Third, all snakes are
obligate carnivores, and most eat relatively large prey that are
frequently dispersed, are vagile, and have large home ranges.
Fourth, snakes average larger body masses than lizards in compa-
rable habitats and often live at much lower densities than lizards
(the exceptions are extreme temperate habitats where snakes, such
as garter snakes and vipers, are more frequent). We conclude that
an ancestral evolutionary environment with a low encounter rate
with both prey and conspecifics is a likely scenario for the evolu-
tion of snakes as a group and could explain the evolution of these
synapomorphies.
Retention of a polygynous mating system from the ancestral
lizard was not likely in the earliest snakes because of the difficulty
of finding or monopolizing females in a fossorial existence. A
male might not easily find more than one female in a season thanks
to the high costs of locomotion, the low rate of moving, the
predation risk associated with surface searches, and the possibly
high dispersion of females. This also offers an explanation for the
switch in SSD from male biased to female biased. Perhaps the
ancestral snake did not have male–male combat, which is present
in virtually all lizards (Pianka & Vitt, 2003). Territoriality, which
is present in most lizards, is reduced in the more chemosensory-
dominated Autarchoglossa lizard lineages from which snakes ap-
parently evolved and is undocumented in the most basal snake
families. However, male lizards are still almost always larger, even
in those groups of lizards that show monogamy (Pianka & Vitt,
2003). So, although the benefits of large size in female snakes
continued (larger clutches, increased survival, wide range of prey),
the costs of a male snake being large outweighed the benefits.
Instead, being small was adequate and reduced metabolic ex-
penses, including costs of locomotion for feeding and finding
females. The probability of encountering other males with females
during the reproductive season was so small that male combats
were no longer a major selection pressure for the evolution or
maintenance of large size. Additional support for the importance of
the fossorial environment driving the system is found in the
fossorial slow-worm lizard (Anguis fragilis), which displays
female-biased SSD and multimale breeding aggregations (R.
Platenberg, personal communication, August 2000).
We hypothesize that the ancestral condition of the snakes was
female-biased SSD based on the general trend found in the group
(Shine, 1994). Shine (1994) concluded that the most common
scenario is female-biased SSD except in those cases in which
males combat. Shine stopped short of hypothesizing that female-
biased SSD was the ancestral condition, perhaps being unable to
explain how it could have evolved from an ancestor with male-
biased SSD and a polygynous mating system. We conclude that the
original serpent mating system was not polygyny, as the ancestral
lizards probably had a mating system somewhere between serial
monogamy (when encounter rates were very low) and polyandry
(if several males found the same female).
Parthenogenesis by females is expected to evolve in a situation
of low encounter rate between males and female. It is interesting
to note that the only obligatorily parthenogenetic snake is the blind
snake (Ramphotyplops braminus), a basal snake that has a fossorial
existence (Nussbaum, 1980). Further support for the idea of low
encounter rate in the evolution of snakes is the fact that several
snakes have been documented to show either long-term sperm
storage or even facultative parthenogenesis (Schuett et al., 1997),
including Burmese pythons (Python molurus bivittatus; Groot,
Bruins, & Breeuwer, 2003). Both traits are expected to evolve in
conditions of low encounter rate. Although today, many advanced
(Macrostomata) snake species breed in multimale breeding aggre-
gations, this does not challenge our suggestion that low male–
female encounter rate was the ancestral condition. It is more likely
a derived trait arising after the evolution of the streptostylic jaw
that allowed snakes to successfully swallow large prey equaling
50% or more of their body mass. This low encounter rate with
potential mates was not evident to early snake biologists (most of
451
SNAKE MATING BEHAVIOR
them native to temperate zones) because congregations of north
temperate snakes at hibernacula suggested a different scenario. So,
their interpretation might have been biased to the particular sce-
nario of a very common temperate snake and not something
representative of the whole taxa. Even so, the high concentrations
of common garter snakes in some parts of their extreme northern
range are exceptional judging by the low occurrence of such
aggregations across related taxa and even other populations of this
most widely distributed species. Although northern hibernacula
provide scientists a great opportunity to gather abundant informa-
tion in a short time, these situations are most certainly highly
derived and unrepresentative.
We endorse the call of several authors (Madsen & Shine, 1993c;
Seigel & Ford, 1987; Shine, 1993; Weatherhead et al., 1995) for
long-term field studies of individually marked snakes in different
taxa and different geographic regions. These are needed to test and
develop theories regarding mating systems and sexual selection in
snakes. The fossorial basal snake families so little studied (Greene,
1997) need, in particular, to be studied to test the hypotheses
advanced here.
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Received December 31, 2004
Revision received July 7, 2005
Accepted July 9, 2005 䡲
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