Seasonal Timing of Spermatogenesis and Mating in Squamates: A Reinterpretation
The squamates occur in a variety of climates from tropical to Arctic regions. Being poikilotherms, snakes and lizards in temperate regions, and high elevation tropical environments, must adjust their reproductive biology to reproduce at a time that optimizes offspring survival. The two major components of the reproductive cycle in both males and females are gametogenesis and mating. The reproductive cycle of males is the focus of this study. In snakes in temperate climates, sperm production (spermatogenesis) may occur immediately prior to mating (prenuptial spermatogenesis) or following mating (postnuptial spermatogenesis). In postnuptial spermatogenesis, sperm are produced following the mating season and stored in the efferent testicular ducts (primarily the ductus deferens) until the following spring mating season. Given that most recent phylogenetic reconstructions resolve snakes as a monophyletic group of highly specialized lizards, it is generally assumed that lizards have spermatogenic cycles similar to snakes. Lizard spermatogenic cycles are often described as prenuptial or postnuptial. We propose that the major difference between snake and lizard spermatogenic cycles is the presence of postnuptial spermatogenesis in snakes and the absence of true postnuptial spermatogenesis in lizards. Our interpretation of lizard spermatogenic cycles suggests that all lizards have prenuptial spermatogenesis (i.e., sperm are produced immediately prior to mating). If fertilization occurs months after mating, the female, and not the male, stores the sperm until spring ovulation and fertilization. Using a variety of analytical tools, we analyzed the reproductive strategies of snakes and lizards, and we have concluded that they differ in fundamental ways. Most notably, prenuptial spermatogenesis is the ancestral condition for Squamata with continuous spermatogenesis evolving multiple times independently within lizards and snakes. We also found that postnuptial spermatogenesis evolved early in the evolutionary history of snakes but, we argue, has never evolved in lizards. We suggest that the evolutionary origin of snakes may account for the differences observed in snake versus lizard reproductive cycles, and we present a scenario for the evolution of snake reproductive cycles.
Representations of the major patterns of spermatogenic and vitellogenic cycles of snakes in temperate climates. (A) Typical reproductive pattern of North American Crotalidae. (B) Typical reproductive pattern of North American Colubridae, Xenodontidae, and others. Bold solid line represents spermatogenesis, the dashed line represents vitellogenesis, and horizontal boxes represent mating periods. Individual species differ in that they may have only mating season 1, or 2, or both (see Aldridge and Duvall, 2002; Aldridge et al., 2009 for mating seasons of individual species).
Representations of the reproductive cycle of cordylid lizards in temperate climates. Lines/boxes as in Figure 1. (A) Reproductive cycle of Ouroborus cataphractus (Flemming and Mouton, 2002), described as having a prenuptial spermatogenesis. (B) Reproductive cycle of Smaug giganteus (van Wyk, 1995) described as having postnuptial spermatogenesis. In Ouroborus cataphractus, vitellogenesis, spermatogenesis, and the mating period occur in the spring, typical of prenuptial spermatogenesis. In Smaug giganteus, vitellogenesis occurs in the spring, similar to Ouroborus cataphractus; however, spermatogenesis occurs in the summer. Based on limited data, van Wyk (1995) states that mating occurs in the spring (mating box 1). However, other data suggest the mating season occurs in the summer (mating box 2, see text), and the sperm would be stored over winter in the oviduct. If mating is restricted to the summer, this is prenuptial spermatogenesis, whereas, if mating occurs in the spring (with or without the summer mating period), this pattern would be postnuptial spermatogenesis, because sperm would be stored in the efferent ducts of the male over winter.
Plots of climate (left) and mating strategy (right), showing summary from 100 stochastically mapped character histories (pie charts at nodes). Phylogeny from Tonini et al. (2016) with branches colored by a representative history from each of the distributions. Insets show the significant Pagel binary-correlation models between climate and mating strategy for lizards and snakes, illustrating the transition rates between states scaled to the maximum rate across both clades.
Phenograms of lizards (top) and snakes (bottom), showing time-scaled phylogeny from Tonini et al. (2016) with tip height scaled to mean annual temperature for each species' range. The insets show the distribution of estimated correlation between temperature and mating strategy for each clade using the threshold model of Felsenstein et al. (2012). For both groups, the horizontal dashed line at 20°C shows the approximate point at which mating strategies shift, with the majority of lizards with continuous and snakes with continuous or prenuptial spermatogenesis associated with higher temperatures. Of note is the clade of viperine vipers (Vipera) associated with lower temperatures (∼2–15°C) that nonetheless exhibit prenuptial spermatogenesis.
Contributor Notes
Associate Editor: W. L. Smith.