Marine Biology

, 164:179 | Cite as

Self-fertilization and inbreeding depression in three ascidian species that differ in genetic dispersal potential

  • Aimee L. PhillippiEmail author
  • Philip O. Yund
Original paper


Although self-fertilization can mitigate the costs of sexual reproduction, many hermaphroditic marine invertebrates avoid selfing, presumably because of inbreeding depression. Eventually, successive generations of inbreeding are expected to reduce genetic load, but selfing cannot evolve for future benefits. Initial inbreeding costs of selfing could be offset by the immediate benefits of local adaptation and mating assurance, both of which are more likely in species with limited gene flow. We compared the likelihood of selfing and the magnitude of inbreeding depression among three ascidian species (Molgula provisionalis, Ciona intestinalis, and Botryllus schlosseri) that were known a priori to differ in larval dispersal potential. Selfing potential exhibited a negative association, and inbreeding depression a positive association with dispersal potential. M. provisionalis, with highly philopatric larvae, had no apparent barrier to self-fertilization and exhibited little evidence of inbreeding depression (ratio of survival of self to outcross progeny 10 weeks after metamorphosis was 0.999). By contrast, C. intestinalis, with highly dispersive larvae, exhibited low levels of self-fertilization in flowing water and high levels of inbreeding depression (survival ratio 14 weeks after metamorphosis of 0.274). B. schlosseri larvae have intermediate dispersal capabilities, yet exhibited low likelihood of self-fertilization and high magnitude of inbreeding depression (survival ratio 10 weeks after metamorphosis of 0.310); however, extremely long-lived sperm contribute to gene flow in B. schlosseri. These results suggest that in marine hermaphrodites, gene flow, self-fertilization, and inbreeding depression should be evaluated as an integrated suite of traits, not independent characters.



We thank Sheri Johnson, Basma Mohammad, and Beth Ann Choate for laboratory assistance and the National Science Foundation (OCE-01-17623 and OCE-14-58188) for funding.

Compliance with ethical standards


This study was funded by National Science Foundation (OCE-01-17623 and OCE-14-58188).

Conflict of interest

The authors declare they have no conflict of interest.

Ethical approval

All applicable international, national, and institutional guidelines for the care and use of animals were followed.


  1. Antonovics J (1968) Evolution in closely adjacent populations. V. Evolution of self-fertility. Heredity 23:219–238CrossRefGoogle Scholar
  2. Armbruster G, Schlegel M (1994) The land-snail species of Cochlicopa (Gastropoda: Pulmonata: Cochlicopidae): Presentation of taxon-specific allozyme patterns, and evidence for a high level of self-fertilization. J Zool Syst Evol Res 32:282–296CrossRefGoogle Scholar
  3. Barrett SCH (1996) The reproductive biology and genetics of island plants. Phil Trans R Soc Lond B 351:725–733CrossRefGoogle Scholar
  4. Barrett SCH, Charlesworth D (1991) Effects of a change in the level of inbreeding on the genetic load. Nature 352:522–524CrossRefGoogle Scholar
  5. Baur B (1988) Microgeographical variation in shell size of the land snail Chondrina clienta. Biol J Linn Soc 35:247–259CrossRefGoogle Scholar
  6. Ben-Shlomo R (2008) The molecular basis of allorecognition in ascidians. BioEssays 30:1048–1051CrossRefGoogle Scholar
  7. Berrill NJ (1950) The Tunicata. Bernard Quaritch, LondonGoogle Scholar
  8. Bohonak AJ (1999) Dispersal, gene flow, and population structure. Quart Rev Biol 74:21–45CrossRefGoogle Scholar
  9. Brazeau DA, Gleason DF, Morgan ME (1998) Self-fertilization in brooding hermaphroditic caribbean corals: evidence from molecular markers. J Exp Mar Biol Ecol 231:225–238CrossRefGoogle Scholar
  10. Brunetti R, Gissi C, Pennati R, Caicci F, Gasparini F, Manni L (2015) Morphological evidence that molecularly determined Ciona intestinalis type A and type B are different species: Ciona robusta and Ciona intestinalis. J Zool Syst Evol Rev 53:186–193CrossRefGoogle Scholar
  11. Bryant EH, Meffert LM (1990) Multivariate phenotypic differentiation among bottleneck lines of housefly. Evolution 44:660–668CrossRefGoogle Scholar
  12. Byers DL, Waller DM (1999) Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Ann Rev Ecol Syst 30:479–513CrossRefGoogle Scholar
  13. Caplins SA, Turbeville JM (2015) High rates of self-fertilization in a marine ribbon worm (Nemertea). Biol Bull 229:255–264CrossRefGoogle Scholar
  14. Carlon DB (1999) The evolution of mating systems in tropical reef corals. Trends Ecol Evol 12:17–21Google Scholar
  15. Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Ann Rev Ecol Syst 18:237–268CrossRefGoogle Scholar
  16. Charlesworth D, Charlesworth B (1990) Inbreeding depression with heterozygote advantage and its effect on selection for modifiers changing the outcrossing rate. Evolution 44:870–888CrossRefGoogle Scholar
  17. Charlesworth B, Charlesworth D (1999) The genetic basis of inbreeding depression. Genet Res 74:329–340CrossRefGoogle Scholar
  18. Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10:783–796CrossRefGoogle Scholar
  19. Charlesworth D, Morgan MT, Charlesworth B (1990) Inbreeding depression, genetic load and the evolution of outcrossing rates in a multi-locus system with no linkage. Evolution 44:1469–1489CrossRefGoogle Scholar
  20. Cheptou PO, Dieckmann U (2002) The evolution of self-fertilization in density-regulated populations. Proc R Soc Lond B 269:1177–1186CrossRefGoogle Scholar
  21. Crnokrak P, Barrett SCH (2002) Purging the genetic load: a review of the experimental evidence. Evolution 56:2347–2358CrossRefGoogle Scholar
  22. Dart S, Eckert CG (2013) Experimental and genetic analyses reveal that inbreeding depression declines with increased self-fertilization among populations of a coastal dune plant. J Evol Biol 26:587–599CrossRefGoogle Scholar
  23. Dole J, Ritland K (1993) Inbreeding depression in two Mimulus taxa measured by multigenerational changes in the inbreeding coefficient. Evolution 47:361–373CrossRefGoogle Scholar
  24. Dudash MR, Carr DE (1998) Genetics underlying inbreeding depression in Mimulus with contrasting mating systems. Nature 393:682–684CrossRefGoogle Scholar
  25. El-Komi MM, Kajihara T (1991) Breeding and molting of barnacles under rearing conditions. Mar Biol 108:83–89CrossRefGoogle Scholar
  26. Ellison CK, Burton RS (2008) Interpopulation hybrid breakdown maps to the mitochondrial genome. Evolution 62:631–638CrossRefGoogle Scholar
  27. Escobar JS, Auld JR, Correa AC, Alonso JM, Bony YK, Coutellec M-A, Koene JM, Pointier J-P, Jarne P, David P (2011) Patterns of mating-system evolution in animals: correlations among selfing rate, inbreeding depression, and the timing of reproduction. Evolution 65:1233–1253CrossRefGoogle Scholar
  28. Fox C, Scheibly K, Reed D (2008) Experimental evolution of the genetic load and its implications for the genetic basis of inbreeding depression. Evolution 62:2236–2249CrossRefGoogle Scholar
  29. Gandon S (1999) Kin competition, the cost of inbreeding and the evolution of dispersal. J Theor Biol 200:345–364CrossRefGoogle Scholar
  30. Gems D, Riddle DL (1996) Longevity in Caenorhabditis elegans reduced by mating but not gamete production. Nature 379:723–725CrossRefGoogle Scholar
  31. Ghiselin MT (1969) The evolution of hermaphroditism among animals. Quart Rev Biol 44:189–208CrossRefGoogle Scholar
  32. Ghiselin MT (1987) Evolutionary aspects of marine invertebrate reproduction. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of Marine Invertebrates, vol 9, General aspects: seeking unity in diversity. Blackwell Scientific Publications/The Boxwood Press, Palo Alto/Pacific GroveGoogle Scholar
  33. Givinish TJ (2010) Ecology of plant speciation. Taxon 59:1326–1366Google Scholar
  34. Grosberg RK (1987) Limited dispersal and proximity-dependent mating success in the colonial ascidian Botryllus schlosseri. Evolution 41:372–384CrossRefGoogle Scholar
  35. Harada Y, Takagaki Y, Sunagawa M, Saito T, Yamada L, Taniguchi H, Shoguchi E, Sawada H (2008) Mechanism of self-sterility in a hermaphroditic chordate. Science 320:548–550CrossRefGoogle Scholar
  36. Havenhand JN (1991) Fertilisation and the potential for the dispersal of gametes and larvae in the solitary ascidian Ascidia mentula Müller. Ophelia 33:1–15CrossRefGoogle Scholar
  37. Hereford J (2010) Does selfing or outcrossing promote local adaptation? Am J Bot 97:298–302CrossRefGoogle Scholar
  38. Heyward AJ, Babcock RC (1986) Self- and cross-fertilization in scleractinian corals. Mar Biol 90:191–195CrossRefGoogle Scholar
  39. Holsinger KE (1991) Mass-action models of plant mating systems: the evolutionary stability of mixed mating systems. Am Nat 138:606–622CrossRefGoogle Scholar
  40. Holtsford TP, Ellstrand NC (1990) Inbreeding effects in Clarkia tembloriensis (Onagraceae) populations with different natural outcrossing rates. Evolution 44:2031–2046CrossRefGoogle Scholar
  41. Husband BC, Schemske DW (1996) Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50:54–70CrossRefGoogle Scholar
  42. Ianelli F, Pasole G, Sordino P, Gissi C (2007) Mitogenomics reveals two cryptic species in Ciona intestinalis. Trends Genet 23:419–422CrossRefGoogle Scholar
  43. Inoue K (1990) Evolution of mating systems in island populations of Campanula microdonta: pollinator availability hypothesis. Plant Species Biol 5:57–64CrossRefGoogle Scholar
  44. Jain SK (1976) The evolution of inbreeding in plants. Ann Rev Ecol Syst 7:469–495CrossRefGoogle Scholar
  45. James SH (1992) Inbreeding, self-fertilization, lethal genes and genomic coalescence. Heredity 68:449–456CrossRefGoogle Scholar
  46. Jarne P, Auld JR (2006) Animals mix it up too: the distribution of self-fertilization among hermaphroditic animals. Evolution 60:1816–1824CrossRefGoogle Scholar
  47. Jarne P, Finot L, Delay B, Thaler L (1991) Self-fertilization versus cross-fertilization in the hermaphroditic freshwater snail Bulinus globosus. Evolution 45:1136–1146CrossRefGoogle Scholar
  48. Jarne P, Vianey-Liaud M, Delay B (1993) Selfing and outcrossing in hermaphrodite freshwater gastropods (Basommatophora): where, when and why. Biol J Linn Soc 49:99–125CrossRefGoogle Scholar
  49. Jiang D, Smith WC (2005) Self- and cross-fertilization in the solitary ascidian Ciona savignyi. Biol Bull 209:107–112CrossRefGoogle Scholar
  50. Johnson SL, Yund PO (2004) Exceptional sperm longevity in a colonial ascidian. Biol Bull 206:144–151CrossRefGoogle Scholar
  51. Kalisz S, Vogler DW, Hanley KM (2004) Context-dependent autonomous self-fertilization yields reproductive assurance and mixed mating. Nature 430:884–887CrossRefGoogle Scholar
  52. Kawamura K, Fujita H, Nakauchi M (1987) Cytological characterization of self incompatibility in gametes of the ascidian, Ciona intestinalis. Dev Growth Differ 29:627–642CrossRefGoogle Scholar
  53. Kelly RP, Palumbi SR (2010) Genetic structure among 50 species of the northeastern Pacific rocky intertidal community. PLoS One 5:e8594. doi: 10.1371/journal.pone.0008594 CrossRefGoogle Scholar
  54. Knowlton N, Jackson JBC (1993) Inbreeding and outbreeding in marine invertebrates. In: Thornhill NW (ed) The Natural History of inbreeding and Outbreeding. The University of Chicago Press, ChicagoGoogle Scholar
  55. Lambert CC, Brandt CL (1967) The effect of light on the spawning of Ciona intestinalis. Biol Bull 132:222–228CrossRefGoogle Scholar
  56. Lande R, Schemske DW (1985) The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39:24–40CrossRefGoogle Scholar
  57. Larsen L-K, Pélabon C, Bolstad GH, Viken Å, Fleming IA, Rosenqvist G (2011) Temporal change in inbreeding depression in life-history traits in captive populations of guppy (Poecilia reticulata): evidence for purging? J Evol Biol 24:823–834CrossRefGoogle Scholar
  58. Leonard GH, Levine JM, Schmidt PR, Bertness MD (1998) Flow-driven variation in intertidal community structure in a Maine estuary. Ecology 79:1395–1411CrossRefGoogle Scholar
  59. Levin DA (1996) The evolutionary significance of pseudo-self-fertility. Am Nat 148:321–332CrossRefGoogle Scholar
  60. Lloyd DG (1979) Some reproductive factors affecting the selection of self-fertilization in plants. Am Nat 113:67–79CrossRefGoogle Scholar
  61. Lloyd DG (1980) Demographic factors and mating patterns in angiosperms. In: Solbrig OT (ed) Demography and evolution in plant populations. Blackwell, OxfordGoogle Scholar
  62. Mavárez J, Amarista M, Pointier J-P, Jarne P (2000) 0 Microsatellite variation in the freshwater schistosome-transmitting snail Biomphalaria glabrata. Mol Ecol 9:1009–1011CrossRefGoogle Scholar
  63. Maynard Smith J (1971) The origin and maintenance of sex. In: Williams GC (ed) Group selection. Aldine Atherton, ChicagoGoogle Scholar
  64. Maynard Smith J (1978) The evolution of sex. Cambridge University Press, CambridgeGoogle Scholar
  65. McCracken GF, Selander RK (1980) Self-fertilization and monogenic strains in natural populations of terrestrial slugs. Proc Natl Acad Sci 77:684–688CrossRefGoogle Scholar
  66. Milkman R (1967) Genetic and developmental studies on Botryllus schlosseri. Biol Bull 132:229–243CrossRefGoogle Scholar
  67. Millar RH (1953) Ciona. The University Press, LiverpoolGoogle Scholar
  68. Morgan TH (1938) The genetic and the physiological problems of self-sterility in Ciona. I. Data on self- and cross-fertilization. J Exp Zool 78:271–318CrossRefGoogle Scholar
  69. Morgan TH (1942) The genetic and the physiological problems of self-sterility in Ciona. V. The genetic problem. J Exp Zool 90:199–228CrossRefGoogle Scholar
  70. Morgan TH (1944) The genetic and the physiological problems of self-sterility in Ciona. VI. Theoretical discussion of genetic data. J Exp Zool 95:37–59CrossRefGoogle Scholar
  71. Newlon AW III, Yund PO, Stewart-Savage J (2003) Phenotypic plasticity of reproductive effort in a colonial ascidian, Botryllus schlosseri. J Exp Zool 297A:180–188CrossRefGoogle Scholar
  72. Parker MA (1992) Outbreeding depression in a selfing animal. Evolution 46:837–841CrossRefGoogle Scholar
  73. Petersen JK, Svane I (1995) Larval dispersal in the ascidian Ciona intestinalis (L.). Evidence for a closed population. J Exp Mar Biol Ecol 186:89–102CrossRefGoogle Scholar
  74. Phillippi A (2005) A comparative study of self-fertilization in the life histories of three ascidian species with contrasting dispersal patterns. PhD Thesis, University of Maine, OronoGoogle Scholar
  75. Phillippi A, Hamann E, Yund PO (2004) Fertilization in an egg-brooding colonial ascidian does not very with population density. Biol Bull 206:152–160CrossRefGoogle Scholar
  76. Price SC, Jain SK (1981) Are inbreeders better colonizers? Oecologia 49:283–286CrossRefGoogle Scholar
  77. Rea AC, Nasrallah JB (2008) Self-incompatibility systems: barriers to self-fertilization in flowering plants. Int J Dev Biol 52:627–636CrossRefGoogle Scholar
  78. Ribble DO, Miller JS (1992) Inbreeding effects among inbred and outbred laboratory colonies of Peromyscus maniculatus. Can J Zool 70:820–824CrossRefGoogle Scholar
  79. Riginos C, Buckley Y, Blomberg S, Treml E (2014) Dispersal capacity predicts both population genetic structure and species richness in reef fishes. Am Nat 184:52–64CrossRefGoogle Scholar
  80. Rollinson D, Kane RA, Lines JRL (1989) An analysis of fertilization in Bulinus cernicus Gastropoda Planorbidae. J Zool 217:295–310CrossRefGoogle Scholar
  81. Rosati F, DeSantis R (1978) Studies on fertilization in ascidians. I. Self-sterility and specific recognition between gametes of Ciona intestinalis. Exp Cell Res 121:111–119CrossRefGoogle Scholar
  82. Sabbadin A (1971) Self and cross-fertilization in the compound ascidian Botryllus schlosseri. Dev Biol 24:379–391CrossRefGoogle Scholar
  83. Sabbadin A (1982) Formal genetics of ascidians. Am Zool 22:765–773CrossRefGoogle Scholar
  84. Schmitt J, Gamble SE (1990) The effect of distance from the parental site on offspring performance and inbreeding depression in Impatiens capensis: a test of the local adaptation hypothesis. Evolution 44:2022–2030CrossRefGoogle Scholar
  85. Scofield VL, Schlumpberger JM, West LA, Weissman IL (1982a) Protochordate allorecognition controlled by an MHC-like gene complex. Nature 295:499–502CrossRefGoogle Scholar
  86. Scofield VL, Schlumpberger JM, Weissman IL (1982b) Colony specificity in the colonial tunicate Botryllus and the origins of vertebrate immunity. Amer Zool 22:783–794CrossRefGoogle Scholar
  87. Selander RK, Kaufman DW (1973) Self fertilization and genetic population structures in a colonizing land snail. Proc Natl Acad Sci 70:1186–1190CrossRefGoogle Scholar
  88. Selander RK, Ochman H (1983) The genetic structure of populations as illustrated by molluscs. Curr Top Biol Med Res 10:93–123Google Scholar
  89. Shields WM (1982) Philopatry, inbreeding, and the evolution of sex. State University of New York Press, AlbanyGoogle Scholar
  90. Shields WM (1987) Dispersal and mating systems: investigating their causal connections. In: Chepko-Sade BD, Halpin ZT (eds) Mammalian dispersal patterns: the effects of social structure on population genetics. The University of Chicago Press, ChicagoGoogle Scholar
  91. Stewart-Savage J, Yund PO (1997) Temporal pattern of sperm release from the colonial ascidian, Botryllus schlosseri. J Exp Zool 279:620–625CrossRefGoogle Scholar
  92. Stewart-Savage J, Phillippi A, Yund PO (2001) Delayed insemination results in embryo mortality in a brooding ascidian. Biol Bull 201:52–58CrossRefGoogle Scholar
  93. Svane I, Havenhand JN (1993) Spawning and dispersal in Ciona intestinalis (L.). Mar Ecol 14:53–66CrossRefGoogle Scholar
  94. Templeton AR (1986) Coadaptation and outbreeding depression. In: Soulé ME (ed) Conservation biology: the science of scarcity and diversity. Sinauer, SunderlandGoogle Scholar
  95. Van Kleunen M, Manning JC, Pasqualetto V, Johnson SD (2008) Phylogenetically independent associations between autonomous self-fertilization and plant invasiveness. Am Nat 171:195–201CrossRefGoogle Scholar
  96. van Name WG (1945) The North and South American Ascidians. American Museum of Natural History, New YorkGoogle Scholar
  97. Vrijenhoek RC, Graven MA (1992) Population genetics of Egyptian Biomphalaria alexandrina (Gastropoda, Planorbidae). J Heredity 83:255–261Google Scholar
  98. Waller DM (1986) Is there disruptive selection for self-fertilization? Am Nat 128:421–426CrossRefGoogle Scholar
  99. Wells H (1979) Self-fertilization: advantageous or deleterious? Evolution 33:252–255CrossRefGoogle Scholar
  100. Wright S (1977) Evolution and the Genetics of Populations, vol 3. Experimental Results and Evolutionary Deductions. The University of Chicago Press, ChicagoGoogle Scholar
  101. Yund PO, O’Neil PG (2000) Microgeographic genetic differentiation in a colonial ascidian (Botryllus schlosseri) population. Mar Biol 137:583–588CrossRefGoogle Scholar
  102. Yund PO, Stires A (2002) Spatial variation in population dynamics in a colonial ascidian (Botryllus schlosseri). Mar Biol 141:955–963CrossRefGoogle Scholar
  103. Yund PO, Murdock K, Johnson SL (2007) Spatial distribution of ascidian sperm: two-dimensional patterns and short vs. time-integrated assays. Mar Ecol Prog Ser 341:103–109CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Darling Marine Center, School of Marine SciencesUniversity of MaineOronoUSA
  2. 2.Unity CollegeUnityUSA
  3. 3.The Downeast InstituteBealsUSA

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