Roger Downie, Froglife and University of Glasgow
Recently, media outlets summarised the findings of a paper published in Biology Letters (Booth et al., 2023) that reported the first known case of ‘virgin birth’ in a crocodile. Here, I describe the case and put it into the context of other known examples of reproduction without sex in reptiles.
An 18 year old American crocodile (Crocodylus acutus) had been in captivity, in isolation from other crocodiles, in a Costa Rican reptile park since the age of two. To the keepers’ surprise, it produced a clutch of 18 eggs. These were incubated artificially for 3 months, but failed to hatch. They were then opened up: only one contained recognizable contents, a well-developed baby crocodile, sadly dead. Its gonads showed it to be a female, and genetic analysis demonstrated that it was the offspring only of its mother, with no male input.
The technical term for virgin birth, where a female produces offspring without input from a male is ‘parthenogenesis’, and it can be of two general kinds: a) obligate, where it is the only kind of reproduction occurring in that species; b) facultative, where both sexual and non-sexual reproduction can occur.
How common is parthenogenesis? Obligate parthenogernesis is known in about 80 unisexual species of vertebrates, most of them lizards (Neaves and Baumann, 2011). The best-known examples are the whiptail lizards of Mexico and the southern states of USA, with 12 out of over 40 described species of Aspidoscelis (formerly Cnemidophorus) unisexual; and the rock lizards of the Caucasus mountains, with 7 out of 30 Darevskia species unisexual (Spangenburg et al., 2020). The unisexual lizards are nearly all hybrid clones resulting from matings between related species. The unisexual species have either three (triploid) or four (tetraploid) sets of chromosomes which can be identified in terms of the parental species contributing to the cross. It is believed that the unisexual species overcome any disadvantage from the lack of sexual reproduction through the hybrid vigour derived for their extra sets of genes. In Aspidoscelis, Crews et al. (1986) found that the females of unisexual species show female-female courtship behaviour and pseudo-copulation which enhances ovulation.
Obligate parthenogenesis is relatively easy to detect from the complete lack of males in populations of these unisexual species. Facultative parthenogenesis (FP) is more problematic, partly because many species have long-lived sperm which females can retain in their reproductive tracts after mating. The best evidence therefore comes from captive females kept in the absence of males, as in the crocodile case above. It is the first reported example of FP in any crocodilian, and also the first case from a species with temperature-dependent sex determination. In crocodiles, eggs incubated at low and high temperatures develop as females, with males appearing from incubation at intermediate temperatures: the Costa Rican crocodile’s eggs were incubated at 29-300 C, in the female-determining range. FP has been reported from two captive Komodo dragons (Varanus komodoensis) in Chester and London zoos respectively (Watts et al., 2006). The authors note that Komodo dragons kept for the captive breeding of this endangered species are usually housed as single females, with males brought in when the females are in good condition. Their discovery of eggs laid by unmated females (25 eggs, 8 viable in one case; 4 eggs, one viable in the other) may get in the way of the breeding programme. Komodo dragons have ZZ/ZW sex chromosomes, rather than the XX/XY pattern we are more familiar with in mammals. In ZZ/ZW, males are ZZ and females ZW (in XX/XY, males are XY and females XX). Parthenogenetic development from a female Komodo dragon produces ZZ or WW individuals, with ZZ male, and WW probably non-viable. Booth et al. (2012) published the first report of FP in wild snakes: they collected 22 pregnant copperheads (Agkistrodon contortrix) and 37 cottonmouths (A. piscivorus) and examined the litters for signs of FP (few if any male offspring; high proportion developmental failures). Two litters were selected for molecular analysis, to compare the offspring and maternal genomes, and both indicated that they were the products of only the maternal genomes. The authors note that in both cases, one theory for the occurrence of FP did not fit the facts; it has been suggested that females may use FP to overcome a shortage of males in a population, but in neither case was this true. Although unisexuality with obligate parthenogenesis has some advantages over sexual reproduction, it is not clear why FP should occur as an occasional variant on normal sexual reproduction. The finding of FP in a crocodile means that the only reptile taxon where parthenogenesis is unknown is the Chelonia.
The means by which parthenogenesis works as a reproductive mode can be complex. For example, the entry of the sperm into the ripe egg is usually the trigger for development to begin, so how is development triggered in the absence of fertilization? And what happens to the normal chromosomal reduction divisions of meiosis, when no sperm arrives to restore the diploid number? The references to this article will lead you to some of the answers.
You might also ask: does parthenogenesis also occur in amphibians? So far, it has not been reported, but there are unisexual species of amphibians, though they do not reproduce by parthenogenesis: a story for another day.
Booth et al. (2012). Facultative parthenogenesis discovered in wild vertebrates. Biology Letters 8, 983-5.
Booth et al. (2023). Discovery of facultative parthenogenesis in a new world crocodile. Biology Letters 19, 20230129.
Crews et al. (1986). Behavioural facilitation of reproduction in sexual and unisexual whiptail lizards. PNAS 83, 9547-9550.
Neaves and Baumann (2011). Unisexual reproduction among vertebrates. Trends in Genetics 27, 81-88.
Spangenburg et al. (2020). Cytogenetic mechanisms of unisexuality in rock lizards. Scientific Reports 10, 8697.
Watts et al. (2006). Parthenogenesis in Komodo dragons. Nature 444, 1021-2.