Sharks Without Fathers, by Rasha Aridi

It seems like everyday we learn about a species that breaks the rules of biology—warm-blooded sunfish, egg-laying mammals, and air-breathing fish, just to name a few. In this case, sharks have been discovered to reproduce asexually. New research has demonstrated that female sharks can produce viable offspring without the contribution of a male, through a process called parthenogenesis. This discovery has prompted new research as to how females are physiologically able to reproduce this way, the consequences and benefits of parthenogenesis, and how it can be used to promote shark conservation.

Up until 2002, female sharks were not known to produce offspring without males. A “virgin birth” of a bonnethead shark occurred at the Henry Doorly Zoo, prompting scientists at the Belle Isle Aquarium to monitor their white-spotted bamboo shark, Chiloscyllium plagiosum, who had been producing oviposited egg cases over a period of six years. C. plagiusum deposited seven eggs that were saved and incubated; four of them developed into embryos (Feldheim, 2010).  This observation set off a series of research projects and case studies on the virgin births of sharks. Now, parthenogenesis has been described in four captive shark species: the bonnethead, blacktip, zebra, and white-spotted bamboo sharks (Feldheim, 2016). 

Parthenogenic zebra shark pup hatched and reared by the Burj Al Arab Aquarium Team. Source. 

The term “parthenogenesis” describes how females can reproduce from an ovum without fertilization. Usually, especially in vertebrates, one diploid gametocyte duplicates its chromosomes and splits them, forming four gametes that would later form a zygote if fertilization occurs. However, parthenogenesis can produce offspring without mating. There are two types: apomictic and automictic. In the first, common in plants, gametocytes undergo mitosis instead of meiosis; offspring are clones of the mother. In automictic parthenogenesis, which is more common in vertebrates, one gamete becomes the ovum and receives cytoplasm and nutrients. The remaining gametes become polar bodies. Typically, the polar bodies dissolve but, in this case, they fuse with the ovum. This sets off embryonic development. Each polar body is genetically different from the other and the ovum because of chromosomal crossing over between the mother’s paternal and maternal chromatids. Therefore, the offspring of parthenogenesis are not clones of the mother (Holtcamp, 2009). As little as half of genetic material is passed from the mother, which can increase homozygosity but also decrease genetic diversity (Portnoy, 2014). This can have positive and negative effects on the offspring.

After the virgin birth of a bonnethead in 2002, it was hypothesized that the female had somehow managed to mate or store sperm. This was disproved using DNA testing and the fact that the females had been isolated from males for the entirety of their lifetimes. Mahmood Shivji and Demian Chapman used amplified fragment length polymorphism (AFLP) fingerprinting to study the pup’s genome, looking for paternal genes. They found that everything in the DNA profile was from the mother (Holtcamp, 2009). Scientists theorized that because the females were not exposed to males, their bodies managed to produce offspring in an alternative way because only isolated females underwent parthenogenesis to produce pups. This demonstrates that elasmobranchs are able to adapt, and completely alter, their reproductive strategy to suit their environmental circumstances (Dudgeon, 2017).

How parthenogenesis occurs in sharks compared to normal fertilization. H. Fletcher.  Source. 

Parthenogenesis can have detrimental consequences on sharks, on a genetic level and a population level. First of all, parthenogenesis is comparable to inbreeding because it reduces genetic diversity. The offspring are at least half genetically similar to their mothers and there is high homozygosity. In fact, elevated levels of homozygosity are the first indication of parthenogenesis. This puts individuals at risk of physiological defects, making them less suited for their environments (Dudgeon, 2017). Additionally, parthenogenesis typically produces much fewer number, usually just 1-3, of offspring instead of the fifteen pups per litter that mothers are able to produce. (Holtcamp, 2009). This can be devastating to populations, especially when they are at risk of harvesting. Inversely, there are positive effects of parthenogenesis on the mother and offspring. The ability for a female to reproduce by herself is helpful in times when males are unavailable or the female is isolated. (Holtcamp, 2009). Unfortunately, this has become a real problem in wild populations because of human interference and the effects of harvesting on populations. Genetically, asexual reproduction can accelerate the loss of deleterious recessive alleles in inbred populations, but this can be dangerous in wild populations because it reduces genetic diversity (Portnoy, 2014).

The surprising observation for virgin births in chondrichthyes has opened new doors for research and conservation. In this case, viable offspring were produced and studies were done to explain how this occurred and its significance in the sharks’ life history. Both positive and negative consequences were observed, but there was a decrease in genetic variation and an increase in homozygosity. The most significant outcome of this research is how sharks’ reproductive strategies are reflective of their environmental circumstances, which pertains to conservation. Wild sharks are now being studied and observed for signs of parthenogenesis because scientists think that this biological process is more common in nature g than once believed (Holtcamp, 2009). Although it would be fascinating to observe parthenogenesis in wild populations, it is an indicator that the shark population is in trouble. 100 million sharks are killed annually, putting a strain on populations. Furthermore, males and females typically do not interact in the wild, except for mating. Coupled with the fact that they are isolated and shark fisheries typically harvest at a specific location, it is possible for an entire sex to be wiped out in a region (Holtcamp, 2009). When females are ready to mate, they will not have a sufficient group to choose from. If wild females are reproducing via parthenogenesis, it indicates that males are not present in the population or are not suitable. Scientists are now examining if parthenogenesis is an “evolutionary significant alternative to sexual reproduction” (Straube, 2016), instead of a last-resort reproductive means. In conclusion, parthenogenesis provides insight into the environmental circumstances and the sexual history of female sharks. This data can be used to better understand what happens at a genetic and population level, which can improve how sharks are conserved and what scientists can do to better protect them and their ecosystems.

References

Dudgeon, C. L., L. Coulton, R. Bone, J. R. Ovenden, and S. Thomas. 2015. Switch from sexual to parthenogenetic reproduction in a zebra shark. Scientific Reports 7  40537 doi:10.1038/srep40537

Feldheim, K. A., A. Clews, A. Henningsen, L. Todorov, C. Mcdermott, M. Meyers, J. Bradley, A. Pulver, E. Anderson, and A. Marshall. 2016. Multiple births by a captive swellshark Cephaloscyllium ventriosum via facultative parthenogenesis. Journal of Fish Biology 90(3):1047–1053.

Feldheim, K. A., D. D. Chapman, D. Sweet, S. Fitzpatrick, P. Prodhol, M. Shivji, B. Snowden. 2010. Shark virgin birth produces multiple, viable offspring. J Hered: 374-377.

Holtcamp W. 2009. Lone parents: parthenogenesis in sharks.  BioScience 59(7): 546-550. DOI: 10.1525/bio.2009.59.7.3

Portnoy, D. S., C. M. Hollenbeck, J. S. Johnston, H. M. Casman, and J. R. Gold. 2014. Parthenogenesis in a whitetip reef sharkTriaenodon obesusinvolves a reduction in ploidy. Journal of Fish Biology 85(2):502–508.

Straube, N., K. P. Lampert, M. F. Geiger, J. D. Weiß, and J. X. Kirchhauser. 2016. First record of second-generation facultative parthenogenesis in a vertebrate species, the whitespotted bambooshark Chiloscyllium plagiosum. Journal of Fish Biology 88(2):668–675.