Twins! Microsatellite analysis of two embryos within one egg case in oviparous elasmobranchs
Autoři:
Samantha A. Hook aff001; Syafiq M. Musa aff001; Daniel M. Ripley aff001; Jean-Denis Hibbitt aff004; Bianka Grunow aff005; Timo Moritz aff006; Holly A. Shiels aff001
Působiště autorů:
Faculty of Biology, Medicine and Health, University of Manchester, Manchester, United Kingdom
aff001; School of Earth and Environmental Sciences, University of Manchester, Manchester, United Kingdom
aff002; School of Environmental and Natural Resource Sciences, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, Selangor, Malaysia
aff003; SEA LIFE Programmes and Engagement, SEA LIFE Weymouth, Weymouth, United Kingdom
aff004; Leibniz-Institute of Farm Animal Biology, Dummerstorf, Germany
aff005; Deutsches Meeresmuseum, Stralsund, Germany
aff006; Institut für Zoologie und Evolutionsforschung, Friedrich-Schiller-Universität Jena, Germany
aff007
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0224397
Souhrn
Elasmobranchs display various reproductive modes, which have been key to their evolutionary success. In recent decades there has been a rise in the number of reported cases of foetal abnormalities including fertilised, double-embryos held within one egg capsule, hereafter referred to as twins. Previously, the occurrences of twin egg cases have been reported in two batoid and one shark species. We report the first cases of twins in three species of oviparous elasmobranchs: the undulate ray (Raja undulata), the nursehound (Scyliorhinus stellaris), and the small-spotted catshark (Scyliorhinus canicula). We investigated the genetic relationships between the twins in S. stellaris, and S. canicula using microsatellite markers. Whilst the S. stellaris twins displayed the same genotypes, we found that the S. canicula twin individuals arose through heteropaternal superfecundation. This is the first reported incidence of such a paternity in elasmobranchs. The relationship between environmental change and reproductive strategy in elasmobranchs is unclear and further research is needed to determine its effect on the prevalence and mechanisms of formation of elasmobranch twins.
Klíčová slova:
Elasmobranchii – Embryos – Microsatellite loci – Sharks – Twins – Yolk sac – Skates and rays – Clutches
Zdroje
1. Naylor GJP, Caira JN, Jensen K, Rosana KAM, White WT, Last PR. A DNA sequence–based approach to the identification of shark and ray species and its implications for global elasmobranch diversity and parasitology. Bull Am Museum Nat Hist. 2012;367(367):1–262.
2. Compagno LJ V. Checklist of living Chondrichthyes. Reprod Biol phylogeny Chondrichthyes sharks, batoids chimaeras. 2005;503–48.
3. Naylor G, Fedrigo O, Andrés López J. Phylogenetic Relationships among the Major Lineages of Modern Elasmobranchs. 2005
4. Carrier J, Musick J, Heithaus M. Biology of Sharks and Biology of Marine Birds. 2004. 487–521 p.
5. Henningsen AD, Smale M, Garner R, Kinnunen N. Reproduction, Embryonic Development, and Reproductive Physiology of Elasmobranchs. In: Elasmobranch Husbandry Manual: Captive Care of Sharks, Rays, and their Relatives. Ohio Biological Survey; 2004. p. 227–36.
6. Carrier JC, Musick JA, Heithaus MR. Biology of sharks and their relatives. Taylor & Francis Group; 2012. 633 p.
7. Dulvy NK, Simpfendorfer CA, Davidson LNK, Fordham S V., Bräutigam A, Sant G, et al. Challenges and Priorities in Shark and Ray Conservation. Curr Biol. 2017;27(11):R565–72. doi: 10.1016/j.cub.2017.04.038 28586694
8. Hamlett W, Knigth DP, Pereira F, Steele J, Sever M. Oviducal glands in chondrichthyans. In: Reproductive biology and phylogeny of chondrichthyes: sharks, batoid and chimaeras. Enfield: Science Publishers Inc; 2005. p. 301–36.
9. Last P, White W, de Carvalho M, Séret B, Stehmann M, Naylor G. Rays of the World. 1st Edition. Australia: CSIRO Publishing; 2016. 790 p.
10. Compagno LJ V. Alternative life-history styles of cartilaginous fishes in time and space. Environ Biol Fishes. 1990;28(1–4):33–75.
11. Dodd JM. Reproduction in Cartilaginous Fishes (Chondrichthyes). Vol. 9, Fish Physiology. Academic Press; 1983
12. Ellis JR, Shackley SE. The reproductive biology of Scyliorhinus canicula in the Bristol Channel, U.K. J Fish Biol. 1997;51(2):361–72.
13. Coelho R, Erzini K. Reproductive aspects of the undulate ray, Raja undulata, from the south coast of Portugal. Fish Res. 2006;81(1):80–5.
14. Serra-Pereira B, Figueiredo I, Leonel &, Gordo S. Maturation of the Gonads and Reproductive Tracts of the Thornback Ray Raja clavata, with Comments on the Development of a Standardized Reproductive Terminology for Oviparous Elasmobranchs. Ivone Figueiredo & Leonel Serrano Gordo. 2011;3(1):160–75.
15. Richards S., Merriman D., Calhoun L. The biology of the little skate, Raja erinaecea Mitchell. Stud Mar Resour South New England IX Bull Bingham Oceanogr Collect. 1963;18(3):5–67.
16. Jañez JA, Sueiro MC. Scientific Note Oviposition rate of the fanskate Sympterygia bonapartii (Elasmobranchii, Rajidae) (Müller & Henle, 1841) held in captivity. Vol. 4, Pan-American Journal of Aquatic Sciences. 2009.
17. Farrell ED, Mariani S, Clarke MW. Reproductive biology of the starry smooth-hound shark Mustelus asterias: geographic variation and implications for sustainable exploitation. J Fish Biol. 2010;77(7):1505–25. doi: 10.1111/j.1095-8649.2010.02771.x 21078015
18. Mabragaña E, Lucifora LO, Corbo M de L, Díaz de Astarloa JM. Seasonal Reproductive Biology of the Bignose Fanskate Sympterygia acuta (Chondrichthyes, Rajidae). Estuaries and Coasts. 2015;38(5):1466–76.
19. Ebert DA, Davis CD. Descriptions of skate egg cases (Chondrichthyes: Rajiformes: Rajoidei) from the eastern North Pacific. Zootaxa. 2007;1393:1–18.
20. Ishiyama R. Studies on the rajid fishes (Rajidae) found in the waters around Japan. J Shimonoseki Coll Fish. 1958;7:191–394.
21. Hitz CR. Observations on Egg Cases of the Big Skate (Raja binoculata Girard) Found in Oregon Coastal Waters. J Fish Res Board Canada. 1964;21(4):851–4.
22. Kang H-W, Jo Y-R, Kang D-Y, Jeong G-S, Jo H-S. Spawning Characteristics and Artificial Hatching of Female Mottled Skate, Beringraja pulchra in the West Coast of Korea. Dev Reprod. 2013;17(3):247–55. doi: 10.12717/DR.2013.17.3.247 25949140
23. Howard M. Fecundity, egg capsule size and neonate morphometrics of big skate, Beringraja binoculata (Girard, 1855). In:The Elasmobranch Husbandry Manual II: Recent Advances in the Care of Sharks, Rays and their Relatives Special Publication of the Ohio Biological Survey. Ohio Biological Survey; 2017. p. 451.
24. Jeong C-H, Ishihara H, Treloar M, Bor PH, Senou H, Jeong CH. The Comparative Morphology of Skate Egg Capsules (Chondrichthyes: Elasmobranchii: Rajiformes). Bull Kanagawa prefect Mus Nat Sci. 2012;(41):17–33.
25. Musa SM, Czachur M V, Shiels HA. Oviparous elasmobranch development inside the egg case in 7 key stages. PLoS One. 2018;13(11):e0206984. doi: 10.1371/journal.pone.0206984 30399186
26. Ballard WW, Mellinger J, Lechenault H. A series of normal stages for development of Scyliorhinus canicula, the lesser spotted dogfish (Chondrichthyes: Scyliorhinidae). J Exp Zool. 1993;267(3):318–36.
27. Schneider CA, Rasband WS and Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012. pp. 671. doi: 10.1038/nmeth.2089 22930834
28. ISOLATE II Genomic DNA Kit Product Manual. 2017. Available from: www.bioline.com/isolate
29. Griffiths AM, Casane D, McHugh M, Wearmouth VJ, Sims DW, Genner MJ. Characterisation of polymorphic microsatellite loci in the small-spotted catshark (Scyliorhinus canicula L.). Conserv Genet Resour. 2011;3(4):705–9.
30. QIAGEN Multiplex PCR Kit. 2019. Available from: https://www.qiagen.com/gb/shop/pcr/end-point-pcr-enzymes-and-kits/regular-pcr/qiagen-multiplex-pcr-kit/
31. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P. MICRO-CHECKER: Software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes. 2004;4(3):535–8.
32. Raymond M, Rousset F. An exact test for population differentiation. Evolution (N Y). 1995;49(6):1280–3.
33. Raymond M, Rousset F. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered. 1995;86:248–9.
34. Marshall TC, Slate J, Kruuk LEB, Pemberton JM. Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol. 1998;7(5):639–55 doi: 10.1046/j.1365-294x.1998.00374.x 9633105
35. Jones OR, Wang J. COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour. 2010;10(3):551–5. doi: 10.1111/j.1755-0998.2009.02787.x 21565056
36. Gubili C, Sims DW, Veríssimo A, Domenici P, Ellis J, Grigoriou P, et al. A tale of two seas: contrasting patterns of population structure in the small-spotted catshark across Europe. R Soc Open Sci. 2014;1(3):140175. doi: 10.1098/rsos.140175 26064555
37. Gordon CA, Hood AR, Ellis JR. Descriptions and revised key to the eggcases of the skates (Rajiformes: Rajidae) and catsharks (Carcharhiniformes: Scyliorhinidae) of the British Isles. Zootaxa. 2016;4150(3):255–80. doi: 10.11646/zootaxa.4150.3.2 27515657
38. Luer CA, Walsh CJ, Bodine AB, Wyffels JT. Normal embryonic development in the clearnose skate, Raja eglanteria, with experimental observations on artificial insemination. In: Biology of Skates. Dordrecht: Springer Netherlands; 2007. p. 133–49.
39. Caldeira BF. Morfologia e biometria do desenvolvimento embrionário da raia Sympterygia acuta Garman, 1877 (ElasmobranchiiI; Rajidae). 2006
40. Jañez JA, Meijide FJ, Lucifora LO, Abraham C, Argemi F. Growth and reproduction in captivity unveils remarkable life-history plasticity in the smallnose fanskate, Sympterygia bonapartii (Chondrichthyes: Rajiformes). Neotrop Ichthyol. 2018;16(4).
Článek vyšel v časopise
PLOS One
2019 Číslo 12
- S diagnostikou Parkinsonovy nemoci může nově pomoci AI nástroj pro hodnocení mrkacího reflexu
- Je libo čepici místo mozkového implantátu?
- Pomůže v budoucnu s triáží na pohotovostech umělá inteligence?
- AI může chirurgům poskytnout cenná data i zpětnou vazbu v reálném čase
- Nová metoda odlišení nádorové tkáně může zpřesnit resekci glioblastomů
Nejčtenější v tomto čísle
- Methylsulfonylmethane increases osteogenesis and regulates the mineralization of the matrix by transglutaminase 2 in SHED cells
- Oregano powder reduces Streptococcus and increases SCFA concentration in a mixed bacterial culture assay
- The characteristic of patulous eustachian tube patients diagnosed by the JOS diagnostic criteria
- Parametric CAD modeling for open source scientific hardware: Comparing OpenSCAD and FreeCAD Python scripts
Zvyšte si kvalifikaci online z pohodlí domova
Všechny kurzy