Capstone Presentation Summary
Ingrid Schoonover. November 7, 2021. American University
Capstone Title: An Overview of Reproduction and Development in Rhacodactylus auriculatus
The gargoyle gecko (Rhacodactylus auriculatus) is a large frugivorous lizard from the pacific island of New Caledonia. Historically the New Caledonian ecosystems and their fauna have received little attention by researchers or the public, but recently New Caledonia has been rediscovered as a hotspot for biodiversity and micro-endemism. Despite increasing attention to New Caledonian fauna, the life history and biology of the Giant Gecko species has remained a mystery.
Now I present for the first time an introduction to the reproduction and development of the gargoyle gecko (Rhacodactylus auriculatus), including: (1) breeding behavior, (2) oviposition and eggshell morphology, (3) embryonic development and incubation, and (4) early growth and development. For this research project I reared 11 adult gargoyle geckos under the same conditions to control for confounding factors and simulated the New Caledonian climate to induce natural reproductive behavior. Geckos were introduced as pairs and then either isolated or kept together. I collected data for individual body condition (body mass, snout to vent length, and BMI), clutch information (lay date, relative egg mass, clutch order, fertility rate, incubation length and temperature), offspring information (sex, growth rate, body condition). I performed statistical analysis with linear regression, ANOVA, and ACOVA to determine any significant interactions between the explanatory variables and reproduction/development, the best-fitted models were retained.
Reproduction in Rhacodactylus auriculatus occurs throughout the winter and spring and takes a significant toll on the body condition of the breeding adults; this is followed by a recovery period in the summer through fall during which geckos prioritize bulking up for the next breeding season. Successful reproduction corresponds with periods of increased parental energetic investment, with fertility rates dropping as geckos enter their recovery period. This observation coupled with a decline in the relative mass and fertility of subsequent clutches throughout a breeding season suggests that seasonal reproductive success is limited by energetic reserves in R. auriculatus. Furthermore, following copulation females are able to retain sperm to fertilize up to three viable clutches of offspring which allows for delayed reproduction, increased dispersal, and sperm competition. The gargoyle gecko is a multi-clutching (6.5 clutches per year) species that deposits eggs between the spring in summer in clutches of two eggs. The eggshells are semi-calcareous with a 65% mineral content, this is a novel eggshell strategy compared to the rigid-shelled and flexible-shelled eggshells laid by other gecko species, this intermediate level of mineralization is resistant to desiccation and is possibly an adaptation that has allowed them to utilize arboreal nesting sites. Typical of ectothermic species, the incubation length is a function of temperature and generally lasts from 49 to 114+ days. Offspring emerge weighing 2.6 grams and measuring 39 millimeters in snout to vent length, with hatchling body condition increasing with relative egg mass and maternal body condition. No clear trends were seen with regard to the mode of sexual determination, but it was noted that sex ratios among offspring varied by the maternal identity, perhaps sexual determination in Rhacodactylus auriculatus is a result of genotypic x environmental interaction. I also report the first case of facultative parthenogenesis in Diplodactylidae species with a viable offspring developing from the egg of a virgin Rhacodactylus auriculatus, further research is needed to determine the mechanism involved but terminal fusion automixis is suspected. Initial growth rate in hatchling gargoyle geckos is variable and determined in part by maternal environment and embryonic conditions.
Andrews, Robin. 2017. Novel Eggshell of the New Caledonian Diplodactylid Gecko Species Correlophus ciliatus. Journal of Herpetology. 51(2):173-177.
Mengden, G., and King, M. 1990. Chromosomal Evolution in the Diplodactylinae (Geckkonidae, Reptilia) .2. Chromosomal Variability Between New Caledonian Species. Australian Journal of Zoology. 38(2):219-226.
Lee, Y., Kim, N., and Choi, S. 2018. A comparative study of eggshells of Gekkota with morphological, chemical compositional and crystallographic approaches and its evolutionary implications. PLoS ONE. 13(6):e0199496.
Holleley, C., Sarre, S., O’Meally, D., and Georges, A. 2016. Sex Reversal in Reptiles: Reproductive Oddity or Powerful Driver of Evolutionary Change? Sexual Development. 10:279-287.
Gamble, T., Coryell, J., Ezaz, T., Lynch, J., Scantlebury, D., and Zarkower, D. 2015. Restriction Site-Associated DNA Sequencing (RAD-seq) Reveals an Extraordinary Number of Transitions among Gecko Sex-Determining Systems. Molecular Biology. 32(5):1296-1309.
Caldwell, K. 2012. GEKKO JAPONICUS (Japanese Gecko) DEFORMITY. Herpetological Review. 43(3):485.
Kearney, M., and Shine, R. 2004. Developmental success, stability, and plasticitiy in closely related parthenogenetic and sexual lizards (Heteronotia, Gekkonidae). Evolution. 58(7):1560-1572.
Andrews, R. 2012. Water Vapor Permeability of the Rigid-Shelled Gecko Egg. Journal of Experimental Zoology. 317(A):395-400.
Kearney, M., Fujita, M., and Ridenour, J. 2009. Lost Sex in Reptiles: Constraints and Correlations. Lost Sex. 21:447-468.
Barley, A., Reeder, T., Nieto-Montes de Oca, A., Cole, C., and Thomson, R. 2021. A New Diploid Parthenogenetic Whiptail Lizard from Sonora, Mexico, Is the “Missing Link” in the Evolutionary Transition to Polyploidy. The American Naturalist. 198(2):295-309.
Skipwith, P., Bauer, A., Jackman, T., Sadlier, R. 2016. Old but not ancient: coalescent species tree of New Caledonian geckos reveals recent post-inundation diversification. Journal of Biogeography. 43:1266-1276.
Koch, L., and Meunier, J. 2014. Mother and offspring fitness in an insect with maternal care: phenotypic trade-offs between egg number, egg mass and egg care. BMC Evolutionary Biology. 14:125.
Andrewartha, S., Mitchell, N., and Frappell, P. 2010. Does Incubation Temperature Fluctuation Influence Hatchling Phenotypes in Reptiles? Physiology and Biochemical Zoology. 83(4):597-607.
Whittier, J., Stewart, D., and Tolley, L. 1994. Ovarian and Oviductal Morphology of Sexual and Parthenogenetic Geckos of the Heteronotia binoei Complex. American Society of Ichthyologists and Herpetologists. 1994(2):484-492.
Ghandforoush, Titian. 2016. Identifying locations that optimize the conservation and phylogenetic diversity of endemic squamates in the Grand Sud, New Caledonia. ProQuest Dissertations Publishing. No: 10107853
Gamble, T. 2010. A review of sex determining mechanisms in geckos (Gekkota:Squamata). Sexual Development. 4(1-2):88-103.
Snyder, J., Snyder, L., and Bauer, A. 2010. Ecological observations on the Gargoyle Gecko, Rhacodactylus auriculatus (BAVAY, 1869), in southern New Caledonia. Salamandra. 46(1):37-47.
I added the following to Wikipedia in an attempt to improve public access to scientifically-literate information about reptiles:
- Gargoyle geckos reach sexual maturity between 1.5 to 2 years of age and engage in breeding behaviors in response to environmental cues. Breeding occurs throughout the winter and spring, and during this time adults decline in body condition as a result of energy investment into reproduction. The breeding season is followed by a recovery period during the summer and fall, which is characterized by a gain in mass and decline in reproductive behaviors.
- Reproductive success (as measured by the fertility rate and success of clutches) is highest during the breeding season and declines sharply as adults enter a recovery period. Seasonal clutch order also appears to have a significant influence on clutch fertility and declines with each clutch. These observations combined with a decline in the relative egg mass of each sequential clutch suggest that seasonal reproductive success in gargoyle geckos is constrained by their seasonal energy reserves.
- Gargoyle geckos are also capable of retaining sperm from copulation for delayed fertilization and from stored sperm can produce up to three viable clutches.
- Gargoyle geckos are oviparous and lay clutches of two eggs every 36 days (10 to 70), during the spring and summer they lay on average 6.5 clutches (4 to 11).
- Ingrid Schoonover analyzed the eggshell morphology of 16 gargoyle gecko eggs and reported a high mineralization content of 65% by dry mass, in comparison to other gecko species this is quite unusual and can be considered intermediate to soft-shelled species (low mineralization) and rigid-shelled species (high mineralization). This intermediate level of mineralization means that their eggs are less permeable to water vapor and more resistant to desiccation, which is perhaps an evolutionary adaptation that has allowed them to utilize arboreal nesting sites.
- As is seen in most oviparous ectothermic species, incubation length is dependent on incubation temperature, where increasing the incubation temperature results in shorter incubation lengths and decreasing the incubation temperature results in longer incubation lengths. Hatchlings weigh on average 2.6 grams (1.8 to 3.1 g) and 39 millimeters (35 to 45 mm) in snout to vent length. The growth rate is initially high but declines near sexual maturity. Developmental plasticity is observed in regard to hatchling body condition and initial growth rate: variation in hatchling body mass is influenced by (1) relative egg mass, (2) annual standard deviation in maternal mass, (3) maternal mass at the time of oviposition; and the variation in hatchling growth rate is influenced by (1) hatchling body condition, (2) relative egg mass, (3) maternal body mass and body condition. This means that the maternal environment influences the expression of developmental traits in the offspring of gargoyle geckos, where higher quality (greater body condition) females lay larger eggs and produce faster growing offspring than lower quality females.
- The first case of viable facultative parthenogenesis was reported by Ingrid Schoonover at American University in her presentation "An Overview of Reproduction and Development in Rhacodactylus auriculatus". Parthenogenesis refers to embryonic development that proceeds without the presence of sperm, and in this case was documented in a female that been housed alone for her entire life. Other than an eye deformity this parthenogenetic offspring has been developing normally for six months and appears to be female. However, this phenomenon seems to be a rare occurrence, with only 1 of 19 virgin eggs developing into viable offspring.