What explains genital variation in snakes? A review of the hypotheses of genital coevolution
Abstract
Genitalia can be defining traits for many species with internal fertilization. In general, genitalia of males and females typically coevolve, as copulation is one of the most mechanically direct interactions in biology. Snakes, in particular, have quite complex and elaborate genitalia. Male snakes possess paired copulatory organs, known as hemipenes. There is immense variation in these structures, including spines, scoops, size, and the presence of bilobes. Females accordingly have complementary variation in genital structures. Three hypotheses exist to explain this variation and coevolution: the lock-and-key hypothesis, sexual conflict, and cryptic female choice. In an attempt to identify the main driver of this variation and coevolution, this review will investigate each of these hypotheses to explain genitalia variance, and it will evaluate the primary evidence behind each of them. Present evidence majorly supports the sexual conflict hypothesis and the lock-and-key hypothesis. Ultimately, however, further research on female snake genitalia, and on snake genitalia in general, should be completed, as there are still many unanswered questions.
Introduction
In many animals with external genitalia and internal fertilization, the genitals are often elaborate and unique. Males typically have intromittent copulatory organs, and females have an internal genital tract which receives the male intromittent copulatory organ during copulation. Traditionally, male genitalia have been considered more diverse and variable, compared to female genitalia (Eberhard 1985). Female genitalia have not been considered as variable due to lack of research, primarily due to male researcher bias and the hidden nature of female genitalia (Ah-King et al. 2014; Brennan & Prum 2015). Furthermore, female genitalia can be complicated to study, as they are subject to other selective pressures. The female reproductive tract not only receives the male intromittent copulatory organ during copulation, but it also performs birthing functions, sperm storage, and ovipositing (Brennan & Prum 2015). Despite these multiple functions, female genitalia are still considered variable enough for coevolution to occur (Brennan 2016; Brennan & Prum 2015). When discussing genital coevolution, it is vital to have variation in both the male and the female genitalia.
Genital coevolution occurs when evolutionary changes in one sex’s genitalia drives evolutionary change in the opposite sex’s genitalia (Brennan & Prum 2015). As copulation is one of the most mechanically specific interactions between individuals, genitalia of the male and female must evolve closely together in order for copulation to be successful (Brennan 2016; Brennan & Prum 2015). Initially, Charles Darwin proposed that natural selection influences genital coevolution, as copulation is a function of gamete transfer and is necessary for successful reproduction (Darwin 1871). In addition to natural selection, genital coevolution can occur through other mechanisms, such as sexual selection. Experimental evolution has confirmed that genital coevolution occurs under sexual selection pressures and through mate choice (Simmons & Garcia-Gonzalez 2011). Nonetheless, there are three hypotheses that are frequently used to explain the roots of genital coevolution that incorporate both natural and sexual selection: lock-and-key, sexual conflict, and cryptic female choice.
The lock-and-key hypothesis is the most popularly known hypothesis regarding genital coevolution (Eberhard 2010). This hypothesis proposes that genital coevolution occurs through natural selection in order to prevent hybridization and to reinforce reproductive isolation (Dufour 1844; Eberhard 2010; Shapiro & Porter 1989). This is advantageous because hybridizations can be quite costly, especially for females, as they lose a large investment if they produce an inviable or unfit offspring from mating with a heterospecific male (Eberhard 2010). It can also be costly for males, although to a lesser extent, as they do not typically invest as much in the offspring as females do (Bateman 1948). Thus, the genitalia coevolve to only fit with the lock or key of their own species (Brennan & Prum 2015). Under this hypothesis, the genitalia are expected to have a close mechanical fit during copulation and specific coevolution of genital shape (Brennan & Prum 2015). It would also be expected that this would occur when closely related species are living in sympatry, as this is when the risk of hybridization would be the highest. The lock-and-key hypothesis tends to be refuted, however, as female genitalia are not viewed as variable enough to possess species-specific locks (Eberhard 2010). This claim is largely based on the fact that female genitalia are largely understudied, due to male researcher bias and the hidden nature of female genitalia (Ah-King et al. 2014). However, there is now evidence that demonstrates the falsity in this claim, and that female genitalia are in fact also variable (Simmons 2014). With variation in both male and female genitalia, there is a good foundation for supporting the lock-and-key hypothesis.
Another hypothesis that can explain genital coevolution is sexual conflict, which results in sexually antagonistic coevolution, initiating a coevolutionary arms race. Under this hypothesis, males and females compete for control over reproduction, but the genital adaptations that benefit each sex are detrimental to the opposite sex (Chapman et al. 2002; Eberhard 2010). Sexual conflict may occur through male-male competition for a successful fertilization or through natural selection on female behavior, physiology, or morphology, allowing the female to reduce physical harm or resist coercion (Brennan & Prum 2015). One of the best-known examples of sexually antagonistic coevolution is in waterfowl, where males are forceful in their mating attempts with females; this comes at a disadvantage to the female (Brennan et al. 2007). Males have a corkscrew shaped penis and females have a vagina shaped in a way to prevent coercive mating attempts from the males (Brennan et al. 2007). Here, the genitalia of the male and female waterfowl oppose each other, as they fight to gain control over copulation. It can be expected under this hypothesis that the female genitalia or body would be harmed, but that is not always the case when genitals coevolve through sexual selection.
The final hypothesis that can explain genital coevolution is cryptic female choice (CFC), which operates through sexual selection. Under this hypothesis, genital coevolution occurs because females prefer certain sensory stimuli from male genitalia to facilitate a mate choice or become pregnant (Brennan & Prum 2015). Some features of the male genitalia will be more stimulating, and thus will be selected for (Eberhard 2010). In domestic pigs (Sus domesticus), the females require stimulation from a filament on the male penis in order to become pregnant; if they do not receive this stimulation, such as in artificial insemination, pregnancy rates drop (Bonet et al. 2013). In this case, the female need for stimulation drives the evolution of penis shape. This hypothesis also requires female promiscuity, as females must be choosing from multiple males (Brennan & Prum 2015). Additionally, under this hypothesis, male genitalia should not harm the females, as it may under the sexual conflict hypothesis (Friesen et al. 2014). All these three hypotheses mentioned—lock-and-key, sexual conflict, and cryptic female choice—can be investigated further in snakes—a good model for studying genitalia.
In snakes (class Reptilia; order Squamata), the genitalia are elaborate and unique. Male snakes possess paired intromittent copulatory organs, termed hemipenes, and females accordingly have hemiclitores, as well as vaginal pouches (Gredler et al. 2014). Hemipenes extend from the lateral edges of the cloacal opening when everted (Leal & Cohn 2015). These paired copulatory organs are present in lizards as well, which are also part of the Reptilian order, Squamata. Interestingly, unpaired intromittent copulatory organs are present in two other Reptilian orders, Testudines and Crocodylia, but not the order which contains the tuatara, Rhynchocephalia (Gredler et al. 2014). During embryonic development, hemipenes arise from lateral swellings on each side of the cloaca, and as the embryo develops, these swellings grow to form the right and left hemipenes (Leal & Cohn 2015). These organs undergo further development and differentiation as they transform into their mature form.
Once sexually mature, both male and female snakes have immense genital variation, both in physical structure and appearance. Male snake hemipenes have been photographically documented to have spines, scoops, and bilobes, or to have no complex structures at all (Andonov et al. 2017). Similarly, female genitalia, although still widely understudied in snakes, have some documented variation as well. Female pouch morphologies and vaginal shapes differ among species (Showalter et al. 2014; Siegel et al. 2012). The variation has been documented across many snake species and suggests a close genital coevolution. However, it is still unknown what explains this genital variation and coevolution, and what the main force of evolution is behind it. In an attempt to locate the main driver of this genital variation and coevolution in snakes, this review will investigate each of the hypotheses that explain genital variance and coevolution, and it will evaluate the primary evidence behind each of them. This review will begin with the discussion of evidence behind the classic hypothesis of genital coevolution, the lock-and-key hypothesis. It will then transition into the two other hypotheses, sexual conflict and cryptic female choice, and highlight the evidence behind each of them.