Evidence for viable, non-clonal but fatherless Boa constrictors

Abstract

Parthenogenesis in vertebrates is considered an evolutionary novelty. In snakes, all of which exhibit genetic sex determination with ZZ : ZW sex chromosomes, this rare form of asexual reproduction has failed to yield viable female WW offspring. Only through complex experimental manipulations have WW females been produced, and only in fish and amphibians. Through microsatellite DNA fingerprinting, we provide the first evidence of facultative parthenogenesis in a Boa constrictor, identifying multiple, viable, nonexperimentally induced females for the first time in any vertebrate lineage. Although the elevated homozygosity of the offspring in relation to the mother suggests that the mechanism responsible may be terminal fusion automixis, no males were produced, potentially indicating maternal sex chromosome hemizygosity (WO). These findings provide the first evidence of parthenogenesis in the family Boidae (Boas), and suggest that WW females may be more common within basal reptilian lineages than previously assumed.

Um estudo de caso ligado ao sexo em Python regius (Serpentes: Boidae), com novas ideias sobre a determinação sexual em Henophidia

“…Although sex determination systems are subject to a high degree of evolutionary plasticity (Bachtrog et al 2014), Booth et al's (2011a) observation may be interpreted as evidence that the male is the heterogametic sex, because it demonstrates that the male has the genetic underpinnings necessary to express male and female gonads, whereas, there is no evidence to suggest that the female is capable of producing male gonads. Bergero and Charlesworth (2008) took note that some snakes may have an XX/XY sex chromosome system with only a small nonrecombining region, which has not yet been detected, and this hypothesis is consistent with the case study of CG presented herein, as well as with the cases of TFAP thus far documented in Henophidia (Booth et al 2011a, b, 2014, Kinney et al 2013. A few candidate sex chromosomes exist for Henophidia, based on genomic comparison to sex determining systems in other vertebrates.…”

“…Yet, many species of Caenophidia snakes, as well as lizards and birds, that are well documented as having ZZ/ZW sex determination systems appear to produce only male offspring when reproducing by TFAP, indicating that WW is a non-viable combination in these amniotes (e.g., Olsen and Marsden 1954, Schuett et al 1998, Watts et al 2006, Reynolds et al 2012. With no substantiated evidence of a ZZ/ZW sex determination system in boas and pythons, a more parsimonious interpretation of Booth et al's (2011aBooth et al's ( , b, 2014 and Kinney et al's (2013) observations is that the boas and pythons observed to reproduce by TFAP have an XX/XY sex determination system, and that the half clone parthenogens have the homozygous XX genotype, as does the mother; this would also explain why no males result from these TFAP cases. Booth et al (2011a) also reported observing that male Boa Constrictors produce both male and female gonads during development, whereas females only produce female gonads.…”

“…Booth et al (2011aBooth et al ( , b, 2014 documented the occurrence of facultative parthenogenetic repro-duction in the Boa Constrictor, the Colombian Rainbow Boa (Epicrates maurus), the Ball Python, and the Reticulated Python (Malayopython reticulatus), and Kinney et al (2013) documented facultative parthenogenesis in the Brazilian Rainbow Boa (Epicrates cenchria). In these studies, Booth et al (2011aBooth et al ( , b, 2014 and Kinney et al (2013) genotyped multiple loci of the offspring and demonstrated that the offspring are homozygous throughout the majority of these loci, which the investigators interpreted as indicative of terminal fusion automictic parthenogenesis (TFAP). The parthenogens studied in these case studies were all females; Booth et al (2011a, b) and Kinney et al (2013) interpreted this to mean that these offspring were homozygous for a W sex chromosome.…”

“…Mengden and Stock (1980) reportedly one Dumeril's Boa (Acrantophis dumereli) karyoand, moreover, the investigators were not aware of the phenotypic sex of the individual that was karyotyped. Despite this lack of evidence, investigators have repeatedly assumed that all snakes possess female hetero gamety (e.g., Organ Booth et al 2011a, b, Ashman et al 2014. Even when reporting on karyotypes, FISH mapping, genomes, and gene expression analyses that have all failed to identify sex chromosomes in Henophidia, researchers have interpreted the fourth largest chromosomes of henophidians to be homo morphic sex chromosomes, based on homology to the Z chromosome of the caenophidians (Beçak et al 1964, Ray-Chaudhuri et al 1971, Matsubara et al 2006, O'Meally et al 2010, Vicoso et al 2013.…”

“…With no substantiated evidence of a ZZ/ZW sex determination system in boas and pythons, a more parsimonious interpretation of Booth et al's (2011aBooth et al's ( , b, 2014 and Kinney et al's (2013) observations is that the boas and pythons observed to reproduce by TFAP have an XX/XY sex determination system, and that the half clone parthenogens have the homozygous XX genotype, as does the mother; this would also explain why no males result from these TFAP cases. Booth et al (2011a) also reported observing that male Boa Constrictors produce both male and female gonads during development, whereas females only produce female gonads. Although sex determination systems are subject to a high degree of evolutionary plasticity (Bachtrog et al 2014), Booth et al's (2011a) observation may be interpreted as evidence that the male is the heterogametic sex, because it demonstrates that the male has the genetic underpinnings necessary to express male and female gonads, whereas, there is no evidence to suggest that the female is capable of producing male gonads.…”