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Thursday, February 13, 2014

Snakes that Give Virgin Birth

In continuing association with the group that brought you the #SnakesAtYourService December blog carnival, this post is part of the new Reptile & Amphibian Blogging Network's first event, #HerpsAdapt. Starting on February 12th (in honor of Charles Darwin’s birthday), this event will showcase the remarkable evolutionary abilities of reptiles and amphibians.

One of several excellent new science mnemonics
from the popular webcomic xkcd
Virgin birth (a form of asexual reproduction) has fascinated humans for centuries. Recently, biologists have uncovered many of the mysteries associated with the ability of some animals to produce offspring without ever mating. This phenomenon is common in bacteria, most fungi, many plants, and some invertebrate animals, where it takes many forms. It is relatively uncommon in vertebrates, although a few species of fishes, amphibians, and reptiles reproduce using a form of asexual reproduction called parthenogenesis, which is when an embryo develops from an unfertilized egg cell. Parthenogenesis can be facultative or obligate. Species with facultative parthenogenesis can also reproduce sexually (and usually do), whereas species with obligate parthenogenesis cannot and are usually all-female. Both types of parthenogenesis are found in snakes, and several new examples have been documented in the past few years.

Brahminy Blindsnake (Ramphotyphlops braminus)
Only one species of snake is known to have obligate parthenogenesis. It is a member of the Scolecophidia, or blindsnakes, called the Brahminy Blindsnake or Flowerpot Snake (Ramphotyphlops braminus). This tiny egg-laying species is made up only of females and is extremely widespread, partially thanks to the ability of just a single individual to colonize new areas. Unlike mammals, most reptiles (and birds) have a ZW chromosomal sex determination system, so instead of the males being XY and the females XX (click here for a review), male snakes are ZZ and female snakes are ZW. However, in common with other obligate parthenogenetic species, Brahminy Blindsnakes are triploid, meaning that they have three sets of chromosomes rather than two. Examination of the karyotype (a picture of one complete set of chromosomes) of Brahminy Blindsnakes has revealed evidence of hybridization, which has also played a role in the origin of other polyploid obligate parthenogenetic vertebrates, including certain lizards, salamanders, and fishes.

Boa constrictor (Boa constrictor)
Facultative parthenogenesis has been documented in a number of species of snakes that normally reproduce sexually. Most of the time this takes place when someone has kept a female snake in captivity for a long period of time. Although it can be difficult to distinguish parthenogenesis from long-term sperm storage, which is possible in snakes over periods of up to at least 5 years, new molecular methods have allowed biologists to differentiate offspring that were produced parthenogenetically from those that were produced from sexual reproduction following prolonged sperm storage. Looking back at supposed cases of lengthy sperm storage may reveal facultative parthenogenesis in unexpected places.

In snakes, there are a wide variety of cellular mechanisms by which parthenogenesis can occur. Evidence for the exact type of facultative parthenogenesis can be gained by examining the sex and karyotype of the offspring, and appears to be correlated with the higher taxonomic group. Captive booid snakes such as rainbow boas (Epicrates maurus) and boa constrictors (Boa constrictor) have given birth to viable female offspring that have a WW sex chromosome pair, which is different from any other known chromosome combination. Why the parthenogenetically-produced offspring of these species are not a 50:50 mix of ZW and WW (the two combinations a female boa is capable of making via meiosis) is unknown.

Burmese Python (Python bivittatus)
Burmese python (Python bivittatus) females are capable of making exact ZW female clones of themselves, using a mechanism that is functionally similar to but distinct from that used by obligate parthenogenetic species like the Brahminy Blindsnake. The python offspring are all females and are mostly viable, having suffered no loss of genetic information. In both boas and pythons, the sex chromosomes are monomorphic, meaning that the Z and the W chromosome are approximately equal in size and indistinguishable from one another. It has been suggested that this method of reproduction might help species circumvent limitations on lifespan and establish new populations when individuals are isolated for long periods of time, although this claim will require more evidence to evaluate because parthenogenesis has not been observed in wild boas or pythons. However, new data from molecular ecologist Warren Booth has resulted in a reinterpretation of some of the conclusions of the original description of parthenogenesis in pythons [edit: specifically, Booth & colleagues suggested that the mode is in fact similar in boas and pythons, but that the female python who gave birth to exact clones was herself born via parthenogenesis - which is still exciting because it proves the reproductive competency of parthenogenetically-produced offspring].

Cottonmouth (Agkistrodon piscivorus)
In contrast, facultative parthenogenesis in caenophidians is fraught with difficulties. Most of the offspring produced this way are not viable because they have suffered a loss of some genetic information. Many are stillborn or have deformities or other abnormalities. All are males, and the litters are unusually small. Nevertheless, parthenogenesis has been documented in both captive and wild Cottonmouths (Agkistrodon picivorus) and Copeprheads (Agkistrodon contortrix), and in captive Eastern Diamondback (Crotalus adamanteus), Timber (C. horridus), and Aruba Island (C. unicolor) Rattlesnakes, four species of gartersnakes (Thamnophis couchii, T. elegans, T. marcianus, and T. atratus), and Arafura filesnakes (Acrochordus arafurae). Most of these species are commonly kept in captivity, and they span the gamut from the most basal caenophidians to the most derived, but the infrequent occurrence and low viability of facultative parthenogenesis in these species suggests that although all caenophidians may be capable of parthenogenesis, it is probably not very ecologically or evolutionarily significant. The reproductive potential of the few captive-born parthenogenetically-produced Copperheads that have survived is currently being assessed.

The next steps in this area of herpetology are to discover more about the different cellular and developmental mechanisms that control and influence parthenogenesis, document parthenogenesis in species and taxonomic groups where it is not so far known, and understand more about the hybrid origins of obligate parthenogenetic species. We still don't know what is required to induce parthenogenetic reproduction in either facultative or obligate species - some lizards require copulation with other females, and many salamanders require egg activation by the sperm of a male salamander of a different species. Who knows what bizarre adaptations parthenogenetic snakes await discovery?

Next month: the story of the most widespread snake in the world!

Update: In August 2014 a captive Green Anaconda joined the ranks of boid snakes known to be capable of facultative parthenogenesis, although as of November the observation was still awaiting confirmation via genetic methods. I also learned recently that parthenogenetic snakes play a starring role in a new curriculum for teaching mitosis and meiosis to introductory biology students.


Thanks to xkcd, JD Willson, Todd Pierson, and Pierson Hill for their drawings and photographs.


Booth, W., D. H. Johnson, S. Moore, C. Schal, and E. L. Vargo. 2011. Evidence for viable, non-clonal but fatherless Boa constrictors. Biology Letters 7:253-256 <link>

Booth, W., L. Million, R. G. Reynolds, G. M. Burghardt, E. L. Vargo, C. Schal, A. C. Tzika, and G. W. Schuett. 2011. Consecutive virgin births in the New World boid snake, the Colombian Rainbow Boa, Epicrates maurus. Journal of Heredity 102:759–763 <link>

Booth, W. and G. W. Schuett. 2011. Molecular genetic evidence for alternative reproductive strategies in North American pitvipers (Serpentes: Viperidae): long-term sperm storage and facultative parthenogenesis. Biological Journal of the Linnean Society 104:934–942 <link>

Booth, W., G. W. Schuett, A. Ridgway, D. W. Buxton, T. A. Castoe, G. Bastone, C. Bennett, and W. McMahan. 2014. New insights on facultative parthenogenesis in pythons. Biological Journal of the Linnean Society 10.1111/bij.12286 <link>

Booth, W., C. F. Smith, P. H. Eskridge, S. K. Hoss, J. R. Mendelson, and G. W. Schuett. 2012. Facultative parthenogenesis discovered in wild vertebrates. Biology Letters 8:983-985 <link>

Germano, D. J. and P. T. Smith. 2010. Molecular evidence for parthenogenesis in the Sierra garter snake, Thamnophis couchii (Colubridae). The Southwestern Naturalist 55:280-282 <link>

Groot, T., E. Bruins, and J. Breeuwer. 2003. Molecular genetic evidence for parthenogenesis in the Burmese python, Python molurus bivittatus. Heredity 90:130-135 <link>

Kearney, M., M. K. Fujita, and J. Ridenour. 2009. Lost sex in the reptiles: constraints and correlations. Pages 447-474 in I. Schön, K. Martens, and P. van Dijk, editors. Lost Sex: The Evolutionary Biology of Parthenogenesis. Springer, Dordrecht, Holland <link>

Reynolds, R. G., W. Booth, B. M. Fitzpatrick, G. W. Schuett, and G. M. Burghardt. 2012. Successive virgin births of viable male progeny in the checkered gartersnake, Thamnophis marcianus. Biological Journal of the Linnean Society 107:566–572 <link>

Schuett, G., P. Fernandez, W. Gergits, N. Casna, D. Chiszar, H. Smith, J. Mitton, S. Mackessy, R. Odum, and M. Demlong. 1997. Production of offspring in the absence of males: evidence for facultative parthenogenesis in bisexual snakes. Herpetological Natural History 5:1-10 <link>

Wright, R. 2014. Why Meiosis Matters: The case of the fatherless snake. CourceSource 1:1-6 <link>

Wynn, A. H., C. J. Cole, and A. L. Gardner. 1987. Apparent triploidy in the unisexual brahminy blind snake, Ramphotyphlops braminus. American Museum Novitates 2868:1-7 <link>

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Life is Short, but Snakes are Long by Andrew M. Durso is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License.