Mating Systems, Reproductive Success, and Sexual Selection in Secretive Species: A Case Study of the Western Diamond-Backed Rattlesnake, Crotalus atrox

Abstract

Long-term studies of individual animals in nature contribute disproportionately to our understanding of the principles of ecology and evolution. Such field studies can benefit greatly from integrating the methods of molecular genetics with traditional approaches. Even though molecular genetic tools are particularly valuable for species that are difficult to observe directly, they have not been widely adopted. Here, we used molecular genetic techniques in a 10-year radio-telemetric investigation of the western diamond-backed rattlesnake (Crotalus atrox) for an analysis of its mating system and to measure sexual selection. Specifically, we used microsatellite markers to genotype 299 individuals, including neonates from litters of focal females to ascertain parentage using full-pedigree likelihood methods. We detected high levels of multiple paternity within litters, yet found little concordance between paternity and observations of courtship and mating behavior. Larger males did not father significantly more offspring, but we found evidence for size-specific male-mating strategies, with larger males guarding females for longer periods in the mating seasons. Moreover, the spatial proximity of males to mothers was significantly associated with reproductive success. Overall, our field observations alone would have been insufficient to quantitatively measure the mating system of this population of C. atrox, and we thus urge more widespread adoption of molecular tools by field researchers studying the mating systems and sexual selection of snakes and other secretive taxa.

Bateman-Trivers in the 21st Century: sexual selection in a North American pitviper

“…mammals : Carling, Wiseman & Byers, 2003;birds: Gowaty & Karlin, 1984;fish: Soucy & Travis, 2003); insects (Boomsa, Fjerdingstad & Frydenberg, 1999), and A. contortrix under laboratory conditions (Schuett & Gillingham, 1986)], our findings are novel for wild copperhead, and only the second for New World pitvipers (Jellen & Aldridge, 2011;Clark et al, 2014). Multiple paternity may occur under several scenarios: when females mate multiply within a single season or when long-term sperm storage from different males is maintained across breeding seasons, or a combination of the two (Uller & Olsson, 2008;Jellen & Aldridge, 2011).…”

“…Long-term sperm storage has been documented in A. contortrix and other snakes (Booth & Schuett, 2011) and could result in offspring being sired by males that mated with females in previous seasons. Furthermore, the cryptic coloration and behaviours of many snakes (Shine, 2008), including copperhead, may permit copulation without human detection (Clark et al, 2014), even in well documented and observed populations ).…”

First report on the reproduction of captive Chinese many-toothed snake (Sibynophis chinensis) in Jeju Island, South Korea

“…In early spring, sperms are expelled out from the oviduct to fertilize with oocyte shortly after subsequent spring mating. Many reports have explained that reptiles have two distinct mating seasons prior to ovulation, e.g., Thamnophis sirtalis in Michigan, Bothrops neuwiedi in Brazil, and Crotalus atrox in Arizona (Schwartz et al 1989;Hartmann et al 2004;Clark et al 2014). Fertilization in spring ensures that eggs are laid in the middle of rainy seasons.…”

Male mating success in a North American pitviper: influence of body size, testosterone, and spatial metrics

“…Taxon biases are even found within reptiles, with far less information available on snakes, for instance, than in other lineages (Bonnet, Shine & Lourdais, ; Shine, ). Secretiveness, cryptic habits, rarity, and small body size play a significant role in explaining this historic gap of information in snakes (Bonnet et al ., ; Clark et al ., ). Nonetheless, in recent years, radio‐telemetry has circumvented many logistical problems in locating and observing wild individuals for extended periods (Reinert, ; Dorcas & Willson, ).…”