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Journal of Zhejiang University SCIENCE B 2012 Vol.13 No.10 P.797-810

http://doi.org/10.1631/jzus.B1100152


Absence of postzygotic isolating mechanisms: evidence from experimental hybridization between two species of tropical sea urchins


Author(s):  M. Aminur Rahman, Tsuyoshi Uehara, Aziz Arshad, Fatimah Md. Yusoff, Mariana Nor Shamsudin

Affiliation(s):  Laboratory of Marine Biotechnology, Institute of Bioscience, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia; more

Corresponding email(s):   aminur1963@gmail.com

Key Words:  Sea urchins, Echinometra, Hybridization, Gamete compatibility, Reproductive isolation, Speciation


M. Aminur Rahman, Tsuyoshi Uehara, Aziz Arshad, Fatimah Md. Yusoff, Mariana Nor Shamsudin. Absence of postzygotic isolating mechanisms: evidence from experimental hybridization between two species of tropical sea urchins[J]. Journal of Zhejiang University Science B, 2012, 13(10): 797-810.

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author="M. Aminur Rahman, Tsuyoshi Uehara, Aziz Arshad, Fatimah Md. Yusoff, Mariana Nor Shamsudin",
journal="Journal of Zhejiang University Science B",
volume="13",
number="10",
pages="797-810",
year="2012",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B1100152"
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%T Absence of postzygotic isolating mechanisms: evidence from experimental hybridization between two species of tropical sea urchins
%A M. Aminur Rahman
%A Tsuyoshi Uehara
%A Aziz Arshad
%A Fatimah Md. Yusoff
%A Mariana Nor Shamsudin
%J Journal of Zhejiang University SCIENCE B
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%N 10
%P 797-810
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%D 2012
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B1100152

TY - JOUR
T1 - Absence of postzygotic isolating mechanisms: evidence from experimental hybridization between two species of tropical sea urchins
A1 - M. Aminur Rahman
A1 - Tsuyoshi Uehara
A1 - Aziz Arshad
A1 - Fatimah Md. Yusoff
A1 - Mariana Nor Shamsudin
J0 - Journal of Zhejiang University Science B
VL - 13
IS - 10
SP - 797
EP - 810
%@ 1673-1581
Y1 - 2012
PB - Zhejiang University Press & Springer
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DOI - 10.1631/jzus.B1100152


Abstract: 
Two reef margin species of tropical sea urchins, Echinometra sp. C (Ec) and Echinometra oblonga (Eo), occur sympatrically on Okinawa intertidal reefs in southern Japan. hybridization between these species was examined through a series of cross-fertilization experiments. At limited sperm concentrations, where conspecific crosses reached near 100% fertilization, both heterospecific crosses showed high fertilization rates (81%–85%). The compatibility of the gametes demonstrated that if gamete recognition molecules are involved in fertilization of these species, they are not strongly species-specific. We found that conspecific crosses reached peak fertilization levels much faster than did heterospecific crosses, indicating the presence of a prezygotic barrier to hybridization in the gametes. Larval survival, metamorphosis, and juvenile and adult survival of hybrid groups were nearly identical to those of their parent species. Hybrids from crosses in both directions developed normally through larval stages to sexually mature adults, indicating that neither gametic incompatibility nor hybrid inviability appeared to maintain reproductive isolation between these species. In adults, Ec×Ec crosses gave the highest live weight, followed by Eo (ova)×Ec (sperm), Ec (ova)×Eo (sperm), and Eo×Eo. Other growth performance measures (viz., test size, Aristotle’s lantern length, and gonad index) of hybrid groups and their parental siblings showed the same trends. The phenotypic color patterns of the hybrids were closer to the maternal coloration, whereas spine length, tube-foot and gonad spicule characteristics, pedicellaria valve length, and gamete sizes showed intermediate features. Adult F1 hybrids were completely fertile and displayed high fertilization success in F1 backcrosses, eliminating the likelihood that hybrid sterility is a postzygotic mechanism of reproductive isolation. Conversely, intensive surveys failed to find hybrid individuals in the field, suggesting the lack or rarity of natural hybridization. This strongly suggests that reproductive isolation is achieved by prezygotic isolating mechanism(s). Of these mechanisms, habitat segregation, gamete competition, differences in spawning times, gametic incompatibility or other genetic and non-genetic factors appear to be important in maintaining the integrity of these species.

Darkslateblue:Affiliate; Royal Blue:Author; Turquoise:Article

Reference

[1]Addison, J.A., Hart, M.W., 2005. Colonization, dispersal, and hybridization influence phylogeography of north Atlantic sea urchins (Strongylocentrotus droebachiensis). Evolution, 59(3):532-543.

[2]Arakaki, Y., Uehara, T., 1991. Physiological Adaptation and Reproduction of the Four Types of Echinometra mathaei (Blainville). In: Yanagisawa, T., Yasumasu, I., Oguro, C., Suzuki, N., Motokawa, T. (Eds.), Biology of Echinodermata. A.A. Balkema, Rotterdam, p.105-111.

[3]Arakaki, Y., Uehara, T., 1999. Morphological comparison of black Echinometra individuals among those in the Indo-West Pacific. Zool. Sci., 16(3):551-558.

[4]Arakaki, Y., Uehara, T., Fagoone, I., 1998. Comparative studies of the genus Echinometra from Okinawa and Mauritius. Zool. Sci., 15(1):159-168.

[5]Aslan, L.M., 2000. Comparative Morphological and Ecological Studies of Sympatric Sea Urchins Genus Echinometra in Okinawan Coral Reefs. PhD Thesis, Tohoku University, Sendai, Japan, p.189.

[6]Aslan, L.M., Uehara, T., 1997. Hybridization and F1 backcrosses between two closely related tropical species of sea urchins (genus Echinometra) in Okinawa. Invert. Reprod. Develop., 31(1-3):319-324.

[7]Bartlett, M.S., 1937. Some examples of statistical methods of research in agriculture and applied biology. Suppl. J. Roy. Stat. Soc., 4(2):137-170.

[8]Behrmann-Godel, J., Gerlach, G., 2008. First evidence for postzygotic reproductive isolation between two populations of Eurasian perch (Perca fluviatilis L.) within Lake Constance. Front. Zool., 5(1):3.

[9]Biermann, C.H., Marks, J.A., Vilela-Silva, A.C., Castro, M.O., Mourão, P.A., 2004. Carbohydrate-based species recognition in sea urchin fertilization: another avenue for speciation? Evol. Dev., 6(5):353-361.

[10]Billett, D.S.M., Hausen, B., 1982. Abyssal aggregations of Kolga hyalina Danielssen and Koren (Echinodermata: Holothuroidea) in the northwest Atlantic Ocean: a preliminary report. Deep Sea Res., 29(7):799-818.

[11]Byrne, M., Anderson, M.J., 1994. Hybridization of sympatric Patiriella species (Echinodermata: Asteroidea) in New South Wales. Evolution, 48(3):564-576.

[12]Cameron, R.A., Schroeter, S., 1980. Sea urchin recruitment: effect of substrate selection on juvenile distribution. Mar. Ecol. Prog. Ser., 2:243-247.

[13]Coppard, S.E., Campbell, A.C., 2005. Lunar periodicities of diadematid echinoids breeding in Fiji. Coral Reefs, 24(2):324-332.

[14]Coyne, J.A., 1992. Genetics and speciation. Nature, 355(6360):511-515.

[15]Geyer, L.B., Palumbi, S.R., 2003. Reproductive character displacement and the genetics of gamete recognition in tropical sea urchins. Evolution, 57(5):1049-1060.

[16]Geyer, L.B., Palumbi, S.R., 2005. Conspecific sperm precedence in two species of tropical sea urchins. Evolution, 59(1):97-105.

[17]Howard, D.J., Reece, M., Gregory, P.G., Chu, V., Cain, M.L., 1998. The Evolution of Barriers to Fertilization between Closely Related Organisms. In: Howard, D.J., Berlocher, S.H. (Eds.), Endless Forms: Species and Speciation. Oxford University Press, NY, p.279-288.

[18]Hudson, R.R., Turelli, M., 2003. Stochasticity overrules the “three-times rule”: genetic drift, genetic draft, and coalescence times for nuclear loci versus mitochondrial DNA. Evolution, 57(1):182-190.

[19]Knowlton, N., 1993. Sibling species in the sea. Ann. Rev. Ecol. Syst., 24(1):189-216.

[20]Lamare, M.D., Stewart, B.G., 1998. Mass spawning by the sea urchin Evechinus chloroticus (Echinodermata: Echinoidea) in a New Zealand fiord. Mar. Biol., 132(1):135-140.

[21]Landry, C., Geyer, L.B., Arakaki, Y., Uehara, T., Palumbi, S.R., 2003. Recent speciation in the Indo-West Pacific: rapid evolution of gamete recognition and sperm morphology in cryptic species of sea urchin. Proc. R. Soc. Lond. B, 270(1526):1839-1847.

[22]Lessios, H.A., 1984. Possible prezygotic reproductive isolation in sea urchins separated by the Isthmus of Panama. Evolution, 38(5):1144-1148.

[23]Lessios, H.A., 2007. Reproductive isolation between species of sea urchins. Bull. Mar. Sci., 81(2):191-208.

[24]Lessios, H.A., Pearse, J.S., 1996. Hybridization and introgression between Indo-Pacific species of Diadema. Mar. Biol., 126(4):715-723.

[25]Lessios, H.A., Kessing, B.D., Pearse, J.S., 2001. Population structure and speciation in tropical seas: global phylogeography of the sea urchin Diadema. Evolution, 57(9):2026-2036.

[26]Levitan, D.R., 1998. Does Bateman’s principle apply to broadcast-spawning organisms? Egg traits influence in situ fertilization rates among congeneric sea urchins. Evolution, 52(4):1043-1056.

[27]Matsuoka, N., Hatanaka, T., 1991. Molecular evidence for the existence of four sibling species within the sea urchin, Echinometra mathaei in Japanese waters and their evolutionary relationships (taxonomy and systematics). Zool. Sci., 8(1):121-133.

[28]McCartney, M.A., Lessios, H.A., 2002. Quantitative analysis of gametic incompatibility between closely related species of neotropical sea urchins. Biol. Bull., 202(2):166-181.

[29]Metz, E.C., Palumbi, S.R., 1996. Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin. Mol. Biol. Evol., 13(2):397-406.

[30]Metz, E.C., Kane, R.E., Yanagimachi, H., Palumbi, S.R., 1994. Fertilization between closely related sea urchins is blocked by incompatibilities during sperm-egg attachment and early stages of fusion. Biol. Bull., 187(1):23-34.

[31]Muthiga, N.A., 2003. Coexistence and reproductive isolation of the sympatric echinoids Diadema savignyi Michelin and Diadema setosum (Leske) on Kenyan coral reefs. Mar. Biol., 143(4):669-677.

[32]Nishihira, M., 1975. Spawning of Echinometra mathaei (Blainville) in nature. Sesoko Mar. Sci. Lab. Tech. Rep., 3:11-12.

[33]Nishihira, M., Sato, Y., Arakaki, Y., Tsuchiya, M., 1991. Ecological Distribution and Habitat Preference of Four Types of Echinometra mathaei on Okinawan Coral Reefs. In: Yanagisawa, T., Yasumasu, I., Oguro, C., Suzuki, N., Motokawa, T. (Eds.), Biology of Echinodermata. A.A. Balkema, Rotterdam, p.91-104.

[34]Palumbi, S.R., 1996. What can molecular genetics contribute to marine biogeography? An urchini’s tale. J. Exp. Mar. Biol. Ecol., 203(1):75-92.

[35]Palumbi, S.R., 2009. Speciation and the evolution of gamete recognition genes: patterns and process. Heredity, 102(1):66-76.

[36]Palumbi, S.R., Metz, E.C., 1991. Strong reproductive isolation between closely related tropical sea urchins (genus Echinometra). Mol. Biol. Evol., 8(2):227-239.

[37]Palumbi, S.R., Grabowsky, G., Duda, T., Geyer, L., Tachino, N., 1997. Speciation and population genetic structure in tropical Pacific sea urchins. Evolution, 51:1506-1517.

[38]Pearse, J.S., 1969. Reproductive periodicities of Indo-Pacific invertebrates in the Gulf of Suez. II. The echinoid Echinometra mathaei (de Blainville). Bull. Mar. Sci., 19(3):580-613.

[39]Pearse, J.S., 1998. Distribution of Diadema savignyi and D. setosum in the Tropical Pacific. In: Mooi, R., Telford, M. (Eds.), Echinoderms: San Francisco. A.A. Balkema, Rotterdam, p.777-782.

[40]Pearse, J.S., Philips, B.F., 1968. Continuous reproduction in the Indo-Pacific sea urchin Echinometra mathaei at Rottnest Island, Western Australia. Aust. J. Mar. Freshwat. Res., 19(2):162-172.

[41]Pearse, J.S., Cameron, R.A., 1991. Echinodermata: Echinoidea. In: Giese, A.C., Pearse, J.S. (Eds.), Reproduction of Marine Invertebrates, Vol. VI, Echinoderms and Lophophorates. Boxwood Press, Pacific Grove, CA, p.513-562.

[42]Rahman, M.A., Uehara, T., 2001. Induction of metamorphosis and substratum preference in four sympatric and closely related species of sea urchins (genus Echinometra) in Okinawa. Zool. Stud., 40(1):29-43.

[43]Rahman, M.A., Uehara, T., 2004. Interspecific hybridization and backcrosses between two sibling species of Pacific sea urchins (genus Echinometra) on Okinawan intertidal reefs. Zool. Stud., 43(1):93-111.

[44]Rahman, M.A., Uehara, T., Aslan, L.M., 2000. Comparative viability and growth of hybrids between two sympatric species of sea urchins (genus Echinometra) in Okinawa. Aquaculture, 183(1-2):45-56.

[45]Rahman, M.A., Uehara, T., Pearse, J.S., 2001. Hybrids of two closely related tropical sea urchins (genus Echinometra): evidence against postzygotic isolating mechanisms. Biol. Bull., 200(2):97-106.

[46]Rahman, M.A., Uehara, T., Pearse, J.S., 2004a. Experimental hybridization between two genetically divergent species of tropical sea urchins, Echinometra mathaei and Echinometra oblonga. Invert. Reprod. Develop., 45(1):1-14.

[47]Rahman, M.A., Uehara, T., Hiratsuka, Y., Islam, M.S., 2004b. Hybridization and Gametic Incompatibilities between Two Diverged Species of Indo-Pacific Sea Urchins, Echinometra sp. A and Echinometra mathaei. In: Lee, K.J., Tsai, H.M. (Eds.), Islands of the World VIII International Conference on Changing Islands–Changing Worlds. Kinman Island, Taiwan, p.229-253.

[48]Rahman, M.A., Uehara, T., Lawrence, J.M., 2005. Growth and heterosis of hybrids of two closely related species of Pacific sea urchins (genus Echinometra) in Okinawa. Aquaculture, 245(1-4):121-133.

[49]Strathmann, R.R., 1981. On barriers to hybridization between Strongylocentrotus droebachiensis (O.F. Müller) and S. pallidus (G.O. Sars). J. Exp. Mar. Biol. Ecol., 55(1):39-47.

[50]Tsuchiya, M., Nishihira, M., 1984. Ecological distribution of two types of sea urchin, Echinometra mathaei (Blainville), on Okinawan reef flat. Galaxea, 3:131-143.

[51]Tsuchiya, M., Nishihira, M., 1985. Agonistic behavior and its effect on the dispersion pattern in the two types of the sea urchin, Echinometra mathaei (Blainville). Galaxea, 4:37-48.

[52]Uehara, T., Shingaki, M., 1985. Taxonomic studies in the sea urchin, Echinometra mathaei from Okinawa, Japan. Zool. Sci., 3:1114.

[53]Uehara, T., Asakura, H., Arakaki, Y., 1990. Fertilization Blockage and Hybridization among Species of Sea Urchins. In: Hoshi, M., Yamashita, O. (Eds.), Advances in Invertebrate Reproduction. Elsevier, Amsterdam, p.305-310.

[54]Zar, J.H., 1996. Biostatistical Analysis, 3rd Ed. Prentice Hall International, Inc., Upper Saddle River, NJ.

[55]Zigler, K.S., 2008. The evolution of sea urchin sperm bindin. Int. J. Dev. Biol., 52(5-6):791-796.

[56]Zigler, K.S., Lessios, H.A., 2003. 250 Million years of bindin evolution. Biol. Bull., 205(1):8-15.

[57]Zigler, K.S., Lessios, H.A., 2004. Speciation on the coasts of the new world: phylogeography and the evolution of bindin in the sea urchin genus Lytechinus. Evolution, 58(6):1225-1241.

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