Jesús A. Rivas and Gordon M. Burghardt
Abstract
Sexual selection and mating systems profoundly influence the behavior and psychology of animals. Based on our studies of green anacondas (Eunectes murinus) and a review of other recent studies we conclude that incomplete data derived from a few well-studied snake species has 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 supports the view that polyandry is not only common in snakes but may have been the ancestral mating system. This interpretation helps to explain many of the major and 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 psychological attributes of animals at different taxonomic levels. However, 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 personal biases can cloud scientific judgement (Gowaty, 1994, 1997; Rivas & Burghardt, 2002a; Ruse, 1999; Marsh & Hanlon, 2004). In this contribution we suggest that lack of balanced information about the mating system of different taxa of snakes along with uncritical interpretation of the data at hand have 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 ecological and evolutionary
hypotheses, including those on mating systems (Shine & Bonnet, 2000).
However, despite the fact that there are more than 3000 species of snakes
(Greene, 1997), most of the detailed field and experimental literature dealing
with mating behavior in snakes comes from limited taxonomic groups (e.g. natricines) studied in a limited distribution range (
Polygyny is
typically represented by species where a few males monopolize access to many
females, or in some way manage to gain the benefit of mating with multiple
females, relegating most males in the population to bachelorhood. Classic
representative examples would be northern elephant seals (Mirounga
angustirostris) or the
The influential Emlen and Oring (1977) framework for understanding the diversity of mating systems relied on the degree to which mates could be monopolized, the spatial distribution of resources (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 and 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. Based on their understanding of snake biology, Duvall, Schuett, & Arnold (1993: 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 diagram and list 4 types that they claim encompass virtually all snakes: female defense polygyny (mate guarding), hotspot polygyny, prolonged mate searching polygyny, and explosive mating assemblage polygyny. 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. Polyandry was ignored.
In fact, virtually all reports of mating systems of snakes regard them as polygynous (Duvall, Arnold, & Schuett, 1992; Duvall & Schuett, 1997; Duvall, Schuett, & Arnold, 1993; Shine & Fitzgerald, 1995). Recent papers on snake reproduction that review or expand the evidence of mating systems in snakes continue to use polygyny as a framework to analyze their data (Shine, Langkilde, & Mason, 2003a; Pearson, Shine, & Williams, 2002). However, the requisite multiple matings with several females by individual males per breeding season has been largely assumed (Gibson & Falls, 1975; Schuett, 1982) and seldom documented. Alternatively, a male courting multiple females is considered as evidence of multiple mating by males without confirmation as to whether those courtships were successful (Blanchard & Blanchard, 1942; Brown & Weatherhead, 1999a; Shine & Fitzgerald, 1995; Weatherhead, Barry, Brown, & Forbes, 1995). Other reports document multiple mating by both males and females (Madsen, Shine, Loman, & Hakansson, 1993) or lack 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, Weatherhead, Gibbs, & Brown, 2002). In short, polygyny requires copulation by a male with several females during the reproductive season and such data from the field are sparse (Table 1). Furthermore, few studies have shown that multiple matings lead to males siring offspring in multiple females (Prosser, Weatherhead, Gibbs, & Brown, 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.
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, 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. While 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 (2001a, 2001b, 2002b) reports of polyandry on anacondas are unusual since individual animals were tracked for several years. Interestingly, anacondas are the first species in where the word polyandry was used to describe, and best describes, the mating system observed. It is, perhaps, not the only or the first instance in which polyandry was documented, but was previously unrecognized.
Other than the work by Rivas and Burghardt, the closest that some authors have come to acknowledging polyandry is by using the word “promiscuity” (Shine & Fitzgerald, 1995), but no further discussion is provided. Even in that study all of their findings were analyzed in the light of “female defense polygyny” or “mate-searching polygyny” (p. 496). The work by Prosser, Weatherhead, Gibbs, & Brown (2002) is an exception to this trend as they documented 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 in scientific meetings and conferences (Rivas 1998, Rivas 2000 Rivas & Burghardt 2001b, 2002b) to skeptical audiences. Interestingly, some colleagues aware of our arguments have recently mentioned polyandry when analyzing their work (e.g., Blouin-Demers, Gibbs, & Wheatherhead 2005).
Viewed objectively, we think that virtually all detailed studies of snake reproductive behavior show that their reproductive biology 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 (Table 2). Males searching for and courting females may suffer high mortality in the wild as a result of their mating investment, which further raises the cost of courting several females (Table 2). Male snakes show assortative mating where males seek to mate with the larger, more fertile, or otherwise more attractive females (Table 2). Males thus choose females selectively instead of mating indiscriminately as would be expected in typical examples of polygyny, if they did not make a large reproductive investment per mating. Such male choosiness that conflicts with multiple mating by male snakes is an important selection pressure, since truly polygynous males should maximize the number of mates and minimize courtship duration and investment per mating event.
The ratio of
available females per male or Operational Sex Ratio (OSR)
is far less than one for many snake species (Arnold & Duvall, 1994, prefer
to use the Breeding Sex Ratio (BSR), 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, 1993b; Rivas, 2000; Shine, Langkilde, & Mason, 2003a; 2003b).
A male-biased OSR creates a great potential for
reproductive females to mate multiple times (Barry, Weatherhead,
& 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
has been found in all the species where it has been studied in detail (Table
1). Thus, anaconda polyandry might not be just a rare exception to the
Duvall, Schuett, &
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 our own species, even though we are generally typed as 'moderately polygynous' rather than monogamous.
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 we interpret and direct our research. For instance, there have been several studies that demonstrate that males obtain mating advantages for being larger, yet the males in those species are smaller than the females (Madsen & Shine, 1993a; Weatherhead, Barry, Brown, & Forbes, 1995; Shine et al. 2000). Sexual selection theory predicts that the sexual selection gradient will be stronger in animals that obtain mating advantages from multiple mating. If the males were polygynous they would be under stronger selection pressure (higher sexual selection gradient) than females due to the benefit of mating with multiple females (Arnold & Duvall, 1994) and will therefore grow larger if large size benefits 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 would be lower than in females (Arnold and Duvall 1994). The abundant literature documenting unsuccessful attempts to explain this apparent dilemma (Brown & Weatherhead, 1999a, 1999b; Madsen & Shine, 1993c; Prosser, Weatherhead, Gibbs, & Brown, 2002; Weatherhead, Barry, Brown, & Forbes, 1995; Weatherhead, Gibbs, & Brown 2002) suggests that this is more than a simple issue of terminology.
The
secretive nature of many snakes and other difficulties that snake researchers
have had in obtaining valid data on snake mating behavior has 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 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 (
We conclude that given the available evidence the dominant mating system in snake is not polygyny. The most common mating system in snakes is polygynandry or even polyandry in some cases. We prefer polygynandry instead of promiscuity since the latter really means lack of discrimination and mating with multiple partners does not necessarily involve lack of discrimination for several potential partners might meet the desired standards.
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) contradicts the view that snakes originated in a marine environment (Caldwell & Lee, 1997) and supports early views that snakes as a group evolved in terrestrial environments (Greene & Cundall, 2000), probably in a subterranean (fossorial) habitat (Gans, 1975; Rieppel, 1988; Forstner, Davis, & Arévalo, 1995; Lee, 1997). The constrained mobility of these early snakes in a fossorial environment could account for a lower encounter rate both with mates and prey. In an aquatic habitat it would also be harder for the animals to follow the scent trails and the encounter rate with mates is also expected to be low (Shine, 1993). Thus, a low encounter rate with potential mates seems to be the most likely scenario in the evolutionary history of snakes.
One of the values of comparative studies is to assess what traits are primitive for a clade and which ones are more derived. In trying to understand the evolution of the mating system, since squamate reptiles, other than serpents, have diverse evolutionary lineages, we will focus on the accepted closest extant saurian relatives of snakes, the Varanoidea (monitors, Varanus, Lanthanotus; beaded lizards, Heloderma) (Forstner, Davis, & Arévalo, 1995; Lee, 1997; Pianka & Vitt, 2003). There are several traits of snakes as a group that differ from their sister taxa and that may support or enhance non-polygynous systems, and may be derived from a low encounter rate. For instance, snakes lack the territoriality and male biased Sexual Size Dimorphism (SSD) that is a common trend in their squamate relatives (Stamps 1983; Wikramanayake & Dryden, 1988; Shine 1994a; Phillips, 1995; Pianka & Vitt, 2003). Although territoriality is less marked in Varanoidea than many other groups of lizards (although injurious fights occur), the lack of territoriality of snakes may also relate to the difficulty snakes have in defending feeding or mating sites, since 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 combat, 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 7 most basal families (Schuett, Gergus, & Kraus, 2001), which lead us to conclude that such combat is a derived trait in snakes. There are also a few other important difference 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, vagile, and have large home ranges. Fourth, snakes average larger body masses than lizards in comparable habitats and often live at much lower densities than lizards (the exceptions are extreme temperate habitats where snakes, such as gartersnakes and vipers, are more frequent). We conclude that an ancestral evolutionary environment with a low encounter rate with both prey and co-specific is a likely scenario for the evolution 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 due to the difficulty of finding or monopolizing females in a fossorial existence. A male might not easily find more than one female in a season due to 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, present in virtually all lizards (Pianka & Vitt, 2003). Territoriality; present in most lizards, is reduced in the more chemosensory dominated Autarchoglossa lizard lineages from which snakes apparently 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, while the benefits of large size in female snakes continued (larger clutches, increased survival, wide range of prey), costs for a male snake to be large outweighed the benefits. Instead, being small was adequate and reduced metabolic expenses, 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 multi-male breeding aggregations (Platenberg, personal communication).
We hypothesize that the ancestral condition of the snakes was female biased SSD based on the general trend found in the group (Shine, 1994a). Shine concluded that the most common scenario is female-biased SSD except in those cases where males combat. Shine stops short of hypothesizing that female-biased SSD is the ancestral condition, perhaps being unable to explain how it could have evolved from an ancestor with male-biased SSD with 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. Interestingly, the only obligatory 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), another basal snake (Groot, Bruins, & Breeuwer, 2003). Both traits are expected to evolve in conditions of low encounter rate. Although today many advanced (Macrostomata) snakes species breed in multi-male breeding aggregations, 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 them native to temperate zones), since congregations of north temperate snakes at hibernacula suggested a different scenario. So their interpretation might have been biased to the particular scenario of a very common temperate snake and not something representative on 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. While northern hibernacula provide scientists a great opportunity to gather abundant information in a short time, these situations are most certainly highly derived and unrepresentative.
We endorse the call of several authors (Madsen & Shine, 1993a; Seigel & Ford, 1987; Shine, 1993, Weatherhead, Barry, Brown, & Forbes, 1995) for long term field studies of individually marked animals in different taxa of snakes and different geographic regions. These are needed in order 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 in order to test the hypotheses advanced here.
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