Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Mating system and evidence of multiple paternity in the Antarctic brooding sea urchin Abatus agassizii

Abstract

Broadcasting is the predominant spawning behavior among benthic marine invertebrates, mainly associated with planktotrophic and planktonic lecitotrophic development. Broadcasting allows genetic mixing that should contribute to increase the genetic diversity of a female clutch. Conversely, in brooding species characterized by protected development, oocytes are retained and only sperm is released, which is supposed to limit the number of males that contribute to a female clutch. This spermcasting behavior together with egg retention, unusually frequent among Antarctic marine invertebrates, putatively give brooders low dispersal capacities which may reduce genetic mixing and generate genetic and kinship structure at a small spatial scale. Like many other Antarctic marine benthic invertebrates, the irregular sea urchin Abatus agassizii is a spermcaster that broods its young. In this study, we assessed the genetic diversity among 66 adults using 6 polymorphic microsatellite loci and performed progeny array analyses in order to evaluate the number of mates per female as well as genetic structure at a small spatial scale. A. agassizii exhibited a polyandric system with 2–5 mates per female regardless of population density. Bayesian analyses suggested the absence of genetic structure along our 20-m transect, while relatedness among individuals did not differ from that expected under panmixia. Finally, we conclude that a limited number of males contribute to a female clutch, probably as a consequence of limited sperm dispersal and that movement of adults may be sufficient to avoid kinship structure in the population.

This is a preview of subscription content, log in to check access.

Fig. 1

References

  1. Addison JA, Hart MW (2005) Colonization, dispersal, and hybridization influence phylogeography of North Atlantic sea urchins (Strongylocentrotus droebachiensis). Evolution 59:532–543

  2. Aljanabi SM, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res 25:4692–4693

  3. Arndt A, Smith MJ (1998) Genetic diversity and population structure in two species of sea cucumber: differing patterns according to mode of development. Mol Ecol 7:1053–1064

  4. Avise JC, Tatarenkov A, Liu JX (2011) Multiple mating and clutch size in invertebrate brooders versus pregnant vertebrates. Proc Natl Acad Sci USA 108:11512–11517. doi:10.1073/pnas.1109216108

  5. Belkhir K, Borsa P, Goudet J, Chikhi L, Bonhomme F (1996–09) GENETIX, logiciel sous Windows TM pour la génétique des populations. Montpellier, France

  6. Belkhir K, Castric V, Bonhomme F (2002) IDENTIX, a software to test for relatedness in a population using permutation methods. Mol Ecol Notes 2:611–614

  7. Bishop JDD (1996) Female control of paternity in the internally fertilizing compound ascidian Diplosoma listerianum. I Autoradiographic investigation of sperm movements in the female reproductive tract. Proc R Soc Lond B 263:369–376

  8. Bishop JDD, Pemberton AJ (2006) The third way: spermcast mating in sessile marine invertebrates. Integr Comp Biol. doi:10.1093/icb/icj037

  9. Boissin E, Hoareau TB, Féral JP, Chenuil A (2008) Extreme selfing rates in the cosmopolitan brittle star species complex Amphipholis squamata: data from progeny-array and heterozygote deficiency. Mar Ecol Prog Ser 361:151–159. doi:10.3354/meps07411

  10. Boissin E, Egea E, Féral JP, Chenuil A (2015) Contrasting population genetic structures in Amphipholis squamata, a complex of brooding, self-reproducing sister species sharing life history traits. Mar Ecol Prog Ser 539:165–177. doi:10.3354/meps11480

  11. Buchanan JB (1966) The biology of Echinocardium cordatum (Echinodermata: spatangoida) from different habitats. J Mar biol Assoc UK 46:97–114

  12. Campbell AC, Coppard S, Tudor-Thomas R, D’Abreo D (2001) Escape and aggregation responses of three echinoderms to conspecific stimuli. Biol Bull Woods Hole 201:175–185

  13. Carrea C, Burridge CP, King CK, Miller KJ (2016) Population structure and long-term decline in three species of heart urchins Abatus spp. near-shore in the Vestfold Hills region, East Antarctica. Mar Ecol Progress Series 545:227–238. doi:10.3354/meps11573

  14. Castric V, Bernatchez L, Belkhir K, Bonhomme F (2002) Heterozygote deficiencies in small lacustrine populations of brook charr Salvelinus Fontinalis Mitchill (Pisces, Salmonidae): a test of alternative hypotheses. Heredity 89:27–35. doi:10.1038/sj.hdy.6800089

  15. Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Bio Evol 24:621–631

  16. Chenuil A, Féral J-P (2003) Sequences of mitochondrial DNA suggest that Echinocardium cordatum is a complex of several sympatric or hybridizing species: a pilot study. In: Féral J-P, David B (eds) Echinoderm Research 2001, Proc. 6th Eur. Conf. Echinoderm, Banyuls-sur-mer, France,. Swets & Zeitlinger Publishers, Lisse, NL, pp 15–21

  17. Chenuil A, Gault A, Féral JP (2004) Paternity analysis in the Antarctic brooding sea urchin Abatus nimrodi. A pilot study. Polar Biol 27:177–182

  18. David B, Chone T, Mooi R, De Ridder C (2005) Antarctic echinoidea. Synopses of the Antarctic benthos, vol 10. Koeltz Scientific Books, Königstein

  19. Dayton PK, Robilliard GA, Paine RT, Dayton LB (1974) Biological accommodation in the benthic community at McMurdo Sound, Antarctica. Ecol Monogr 44:105–128

  20. Dell RK (1972) Antarctic Benthos. Adv Mar Biol 10:1–126

  21. Díaz A, González-Wevar C, Maturana CS, Palma AT, Poulin E, Gerard K (2012) Restricted geographic distribution and low genetic diversity of the brooding sea urchin Abatus agassizii (Spatangoidea: Schizasteridae) in the South Shetland Islands: A bridgehead population before the spread to the northern Antarctic Peninsula? Revista Chilena de Historia Natural 86:457–468

  22. Fell HB (1946) The Embriology of the viviparous ophiuroid Amphipholis squamata Delle Chiaje. Trans R Soc N Z 75:419–464

  23. Gil D, Zaixo HE, Tolonaso JE (2009) Brooding of the sub-Antarctic heart urchin, Abatus cavernosus (Spatangoida: Schizasteridae), in southern Patagonia. Mar Biol 156:1647–1657

  24. Gorospe KD, Karl SA (2013) Genetic relatedness does not retain spatial pattern across multiple spatial scales: dispersal and colonization in the coral, Pocillopora damicornis. Mol Ecol 22:3721–3736. doi:10.1111/mec.12335

  25. Grange LJ, Tyler PA, Peck LS (2007) Multi-year observations on the gametogenic ecology of the Antarctic seastar Odontaster validus. Mar Biol 153:15–23. doi:10.1007/s00227-007-0776-z

  26. Grange LJ, Tyler PA, Peck LS (2011) Fertilization Success of the Circumpolar Antarctic Seastar Odontaster validus (Koehler, 1906): a diver-collected study. In: Pollock NW (ed), Portland, ME, p 140

  27. Grosberg RK (1991) Sperm-Mediate gene flow and the genetic structure of a population of the colonial ascidian Botryllus shlosseri. Evolution 45:130–142

  28. Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological Statistics software package for education and data analysis. Paleontología Electrónica 4:9

  29. Havenhand JN, Styan CA (2009) Reproduction and Larvae/Spore types. In: Dürr S, Thomason JC (eds) Biofouling. Wiley-Blackwell, Oxford

  30. Helmuth B, Veit RR, Holberton R (1994) Long-distance dispersal of a subantarctic brooding bivalve (Gaimardia trapesina) by kelp-rafting. Mar Biol 120:421–426

  31. Hoarau G et al (2005) Low effective population size and evidence for inbreeding in an overexploited flatfish, plaice (Pleuronectes platessa L.). Proceed Biol Sci R Soc 272:497–503. doi:10.1098/rspb.2004.2963

  32. Hoffman JI, Clarke A, Clark MS, Peck LS (2013) Hierarchical population genetic structure in a direct developing antarctic marine invertebrate. PLoS ONE 8:e63954. doi:10.1371/journal.pone.0063954

  33. Hunter RL, Halanych KM (2008) Evaluating connectivity in the brooding brittle star Astrotoma agassizii across the drake passage in the Southern Ocean. J Hered 99:137–148. doi:10.1093/jhered/esm119

  34. Iwata Y, Munehara H, Sakurai Y (2005) Dependence of paternity rates on alternative reproductive behaviors in the squid Loligo bleekeri. Mar Ecol Prog Ser 298:219–228

  35. Jadwiszczack P (2007) Rundom projects: an application for randomization and bootstrap testing, version 1.1

  36. Johnson SL, Yund PO (2004) Remarkable longevity of dilute sperm in a free-spawning colonial ascidian. Biol Bull 206:144–151

  37. Johnson SL, Yund PO (2007) Variation in multiple paternity in natural populations of a free-spawning marine invertebrate. Mol Ecol Notes 16:3253–3262

  38. Jones AG (2001) GERUD 1.0: a computer program for the reconstruction of parental genotypes from progeny arrays using multilocus DNA data. Mol Ecol Notes 1:215–218

  39. Jones AG (2005) GERUD 2.0: a computer program for the reconstruction of parental genotypes from half-sib progeny arrays with known or unknown parents. Mol Ecol Notes 5:708–711. doi:10.1111/j.1471-8286.2005.01029.x

  40. Kalinowski ST, Hedrick PW (2001) Inbreeding depression in captive bighorn sheep. Anim Conserv 4:319–324

  41. Kamel SJ, Oyarzun FX, Grosberg RK (2010) Reproductive biology, family conflict, and size of offspring in marine invertebrates. Integr Comp Biol 50(4):619–629

  42. Khasa PD, Newton CH, Rahman MH, Jaquish B, Dancik BP (2000) Isolation, characterization and inheritance of microsatellite loci in alpine larch and western larch. Genome 43:439–448

  43. Konovalov DA, Heg D (2008) A maximum-likelihood relatedness estimator allowing for negative relatedness values. Mol Ecol Resour 8:256–263

  44. Konovalov DA, Manning C, Henshaw MT (2004) KINGROUP: a program for pedirgree relationship reconstruction and kin group assignments using genetic markers. Mol Ecol Notes 4:779–782

  45. Ledoux J-B et al (2012) Fine-scale spatial genetic structure in the brooding sea urchin Abatus cordatus suggests vulnerability of the Southern Ocean marine invertebrates facing global change. Polar Biol 35:611–623

  46. Levitan DR (2004) Density-dependent sexual selection in external fertilizers: variances in male and female fertilization success along the continuum from sperm limitation to sexual conflict in the sea urchin Strongylocentrotus franciscanus. Am Nat 164:298–309

  47. Levitan DR, Petersen C (1995) Sperm limitation in the sea. TREE 10:228–231

  48. Levitan DR, Young CM (1995) Reproductive success in large populations: empirical measures and theoretical predictions of fertilization in the sea biscuit Clypeaster rosaceus. J Exp Mar Biol Ecol 190:221–241

  49. Levitan DR, Sewell MA, Chia F (1992) How distribution and abundance influence fertilization success in the sea urchin Strongylocentrotus franciscanus. Ecology 73:248–254

  50. Liu JX, Avise JC (2011) High degree of multiple paternity in the viviparous Shiner Perch, Cymatogaster aggregata, a fish with long-term female sperm storage. Mar Biol 158:893–901. doi:10.1007/s00227-010-1616-0

  51. Magniez P (1983) Reproductive cycle of the brooding echinoid Abatus cordatus (Echinodermata) in Kerguelen (Antarctic Ocean): changes in the organ indices, biochemical composition and caloric content of the gonads. Mar Biol 74:55–64

  52. Marshall DJ, Evans JP (2005) Does egg competition occur in marine broadcast-spawners? J Evol Biol 18:1244–1252

  53. McCartney MA, Brayer K, Levitan DR (2004) Polymorphic microsatellite loci from the red urchin, Strongylocentrotus franciscanus, with comments on heterozygote deficit. Mol Ecol Notes 4:226–228

  54. Mercier A, Hamel J-F (2008) Depth-related shift in life history strategies of a brooding and broadcasting deep-sea asteroid. Mar Biol 156:205–223. doi:10.1007/s00227-008-1077-x

  55. Mesphoulhé P, David B (1992) Stratégie de croissance d’un oursin subantarctique: Abatus cordatus del îles Kerguelen. CR Acad Sci Paris 314:205–211

  56. Neves EG, Andrade SC, da Silveira FL, Solferini VN (2008) Genetic variation and population structuring in two brooding coral species (Siderastrea stellata and Siderastrea radians) from Brazil. Genetica 132:243–254. doi:10.1007/s10709-007-9168-z

  57. O’Hara TD, England PR, Gunasekera RM, Naughton KM (2014) Limited phylogeographic structure for five bathyal ophiuroids at continental scales. Deep Sea Res Part I 84:18–28. doi:10.1016/j.dsr.2013.09.009

  58. Palma AT, Poulin E, Silva MG, San Martin RB, Muñoz CA, Díaz AD (2007) Antarctic shallow subtidal echinoderms: is the ecological success of broadcasters related to ice disturbance? Polar Biol 30:343–350

  59. Palumbi SR (1994) Genetic divergence, reproductive isolation and marine speciation. Annu Rev Ecol Syst 25:547–572

  60. Paterson IG, Partridge V, Buckland-Nicks J (2001) Multiple Paternity in Littorina obtusata (Gastropoda, Littorinidae) revealed by microsatellite analyses. Biol Bull 200:261–267

  61. Pearse DE, Anderson EC (2009) Multiple paternity increases effective population size. Mol Ecol 18:3124–3127. doi:10.1111/j.1365-294X.2009.04268.x

  62. Pearse JS, McClintock JB (1990) A comparison of reproduction by the brooding spatangoid echinoids Abatus shackletoni and A. nimrodi in McMurdo Sound, Antarctica. Invertebr Reprod Dev 17:181–191

  63. Pearse JS, Mooi R, Lockhart SJ, Brandt A (2009) Brooding and species diversity in the southern ocean: selection for brooders or speciation within brooding clades? Paper presented at the Smithsonian at the poles: contributions to international polar year science

  64. Pemberton AJ, Hughes RN, Manríquez PH, Bishop JDD (2003) Efficient utilization of very dilute aquatic sperm: sperm competition may be more likely than sperm limitation when eggs are retained. Proc R Soc Lond B (Suppl) 270:S223–S226. doi:10.1098/rsbl.2003.0076

  65. Pennington JT (1985) The ecology of fertilization of echinoid eggs: the consequences of sperm dilution, adult aggregation, and synchronous spawning. Biol Bull 169:417–430

  66. Pierrat B, Saucède T, Festeau A, David B (2012) Antarctic, Sub-Antarctic and cold temperature echinoid database. ZooKeys 204:47–52

  67. Poulin E, Feral J-P (1994) The fiction and the facts of Antarctic brood protecting: population genetics and evolution of schizasterid echinoids. In: David G, Féral & Roux (ed) Echinoderms through time. Balkema, Rotterdam, pp 837–844

  68. Poulin E, Féral JP (1995) Pattern of spatial distribution of a brood-protecting schizasterid echinoid, Abatus cordatus, endemic to the Kerguelen Islands. Mar Ecol Prog Ser 118:179–186

  69. Poulin E, Palma AT, Féral J-P (2002) Evolutionary versus ecological success in Antarctic benthic invertabrates. Trends Ecol Evol 17:218–222

  70. Powell DK, Tyler PA, Peck LS (2001) Effect of sperm concentration and sperm ageing on fertilisation success in the Antarctic soft-shelled clam Laternula elliptica and the Antarctic limpet Nacella concinna. Mar Ecol Prog Ser 215:191–200

  71. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure from multilocus genotype data. Genetics 155:945–959

  72. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43(2):258–275

  73. Raymond M, Rousset F (1995) GENEPOP (Version 1.2): population Genetics software for exact test and Ecumenicism. J Hered 86:248–249

  74. Rousset F (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

  75. Sarvesan R (1969) Some observations on parental care in Octopus dollfusi Robson (Cephalopoda: Octopodidae). J Mar bio Ass India 11:203–205

  76. Schatt PS (1985) DGeloppement et croissance embryonnaire de l’oursin incubant Abatus cordatus (Echinoidea: Spatangoidea). Univ, Paris VI

  77. Schatt PS, Féral JP (1991) The brooding cycle of Abatus cordatus (Echinodermata: Spatangoida) at Kerguelen Islands. Polar Biol 11:283–292

  78. Schatt PS, Féral J-P (1996) Completely direct development of Abatus cordatus, a brooding Schizasterid (Echinodermata: Echinoidea) from Kerguelen, With description of Perigastrulation, a hypothetical New Mode of Gastrulation. Biol Bull 190:24–44

  79. Schinner GO, McClintock JB (1993) Structural characteristics of marsupial brood pouches of the antarctic sea urchins Abatus nimrodi and Abatus shackletoni (Echinoidea: Spatangoidea). J Morphol 216:79–93

  80. Seibel BA, Hochberg FG, Carlini DB (2000) Life history of Gonatus onyx (Cephalopoda: Teuthoidea): deep-sea spawning and post-spawning egg care. Mar Biol 137:519–526

  81. Serrao EA, Havenhand JN (2009) Fertilization strategies. In: Marine hard bottom communities: patterns, dynamics, patterns, and change. Springer, Heidelberg

  82. Sewell MA, Hofmann GE (2011) Antarctic echinoids and climate change: a major impact on the brooding forms. Glob Change Biol 17:734–744. doi:10.1111/j.1365-2486.2010.02288.x

  83. Shaw PW, Sauer WHH (2004) Multiple paternity and complex fertilisation dynamics in the squid Loligo vulgaris reynaudii. Mar Ecol Prog Ser 270:173–179

  84. Shuster SM, Wade MJ (2003) Mating systems and mating strategies. Monographs in behavior and ecology. Princeton University Press, Princeton, p 533

  85. Slattery M, Bosch I (1993) Mating behavior of a brooding Antarctic asteroid, Neosmilaster georgianus. Invertebr Reprod Dev 24:97–102

  86. Smilansky V, Lasker HR (2014) Fine-scale genetic structure in the surface brooding Caribbean octocoral, Antillogorgia elisabethae. Mar Biol 161:853–861. doi:10.1007/s00227-013-2385-3

  87. Sui L, Zhang F, Wang X, Bossier P, Sorgeloos P, Hänfling B (2009) Genetic diversity and population structure of the Chinese mitten crab Eriocheir sinensis in its native range. Mar Biol 156:1573–1583

  88. Thompson BAW, Riddle MJ (2005) Bioturbation behaviour of the spatangoid urchin Abatus ingens in Antarctic marine sediments. Marine Ecology Progress Series 290

  89. Tsuruwaka Y, Shimada E (2011) Rearing and spawning of the deep-sea fish Malacocottus gibber in the laboratory. Ichthyol Res 58:188–190

  90. Van de Putte A, Youdjou N, Danis B (2012) The Antarctic biodiversity information facility. World Wide Web publication, available at http://www.biodiversity.aq

  91. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO—CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

  92. Van Oosterhout C, Weetman D, Hutchinson WF (2006) Estimation and adjustment of microsatellite null alleles in nonequilibrium populations. Mol Ecol Notes 6:255–256. doi:10.1111/j.1471-8286.2005.01082.x

  93. Voight JR, Feldheim KA (2009) Microsatellite inheritance and multiple paternity in the deep-sea octopus Graneledone boreopacifica (Mollusca: Cephalopoda). Invertebr Biol 128:26–30

  94. Waples RS, Gaggiotti O (2006) What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol Ecol 15:1419–1439. doi:10.1111/j.1365-294X.2006.02890.x

  95. Weber AA, Merigot B, Valiere S, Chenuil A (2015) Influence of the larval phase on connectivity: strong differences in the genetic structure of brooders and broadcasters in the Ophioderma longicauda species complex. Mol Ecol 24:6080–6094. doi:10.1111/mec.13456

  96. Weir BS, Cockerham CC (1984) Estimating f-statistics for the analysis of population structure. Evolution 38(6):1358–1370

  97. Wright S (1949) The genetical structure of populations. Ann Eugen 15:323–354

  98. Yue GH, Chang A (2010) Molecular evidence for high frequency of multiple paternity in a freshwater shrimp species Caridina ensifera. PLoS ONE 5:e12721. doi:10.1371/journal.pone.0012721

  99. Yund PO (1995) Gene flow via the dispersal of fertilizing sperm in a colonial ascidian (Botryllus schlosseri): the effect of male density. Mar Biol 122:649–654

  100. Yund PO (2000) How severe is sperm limitation in natural populations of marine free-spawners? TREE 15:10–13

  101. Yund PO, McCartney MA (1994) Male reproductive success in sessile invertebrates: competition for fertilizations. Ecology 75:2151–2167

  102. Zar JH (1984) Biostatistical analysis. Prentice-Hall Inc., Nueva York

Download references

Acknowledgments

This study was supported by the Grants PFB-23 and ICM P05-002 and Thesis project INACH M02_10 and CONICYT PhD 21150317 to C.M; INACH D05-09, FP_03-12, CONICYT Ph.D. D-21060218, D21-08 and Postdoctoral FONDECYT 3130677 to A.D, Fondecyt post-doctorate 3100139 and INACH F01_09 to K.G and Egide program ECOS-Sud C06B02 to E.P. and J-P.F.

Author information

Correspondence to Claudia S. Maturana.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Maturana, C.S., Gérard, K., Díaz, A. et al. Mating system and evidence of multiple paternity in the Antarctic brooding sea urchin Abatus agassizii . Polar Biol 40, 787–797 (2017). https://doi.org/10.1007/s00300-016-2001-3

Download citation

Keywords

  • Parentage analysis
  • Polyandry
  • Spermcast
  • Vagility
  • Panmixia