Paternity and gregariousness in the sex-changing sessile marine gastropod crepidula convexa: Comparison with other protandrous crepidula species

Journal of Heredity

Volumn 105, Issue 3, 2014, Pages 397-406

  Le Cam, Sabrina ^a,b   Riquet, Florentine ^a,b   Pechenik, Jan A ^c   Viard, Frédérique ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b STATION BIOLOGIQUE   (France)

^c TUFTS UNIVERSITY   (United States)

Author keywords

Gregarity; microsatellite; mollusc; paternity analysis; protandry

Indexed keywords

ADULT; AGE DISTRIBUTION; ANIMAL BEHAVIOR; ANIMAL STRUCTURES; ARTICLE; CREPIDULA CONVEXA; CREPIDULA COQUIMBENSIS; CREPIDULA FORNICATA; DNA EXTRACTION; EMBRYO; FEMALE; GASTROPOD; GENETIC VARIABILITY; GENOTYPE; MALE; MICROSATELLITE MARKER; NONHUMAN; PATERNITY; POLYANDRY; PRIORITY JOURNAL; PROTANDRY; SEX DIFFERENTIATION; SEX TRANSFORMATION; SEXUAL DYSFUNCTION; STRUCTURE ANALYSIS; ANIMAL; FERTILIZATION; GENETICS; LIFE CYCLE STAGE; POPULATION GENETICS; SEX DETERMINATION PROCESS; SEXUAL BEHAVIOR; SEXUAL DEVELOPMENT; ANIMAL EXPERIMENT; FATHER; HETEROZYGOTE; LIFE HISTORY; MARINE SNAIL; NULL ALLELE; PARENTHOOD; PROGENY; SPECIES COMPARISON;

MICROSATELLITE DNA;

ANIMALS; FEMALE; FERTILIZATION; GASTROPODA; GENETIC VARIATION; GENETICS, POPULATION; GENOTYPE; LIFE CYCLE STAGES; MALE; MICROSATELLITE REPEATS; PATERNITY; SEX CHARACTERISTICS; SEX DETERMINATION PROCESSES; SEXUAL BEHAVIOR, ANIMAL;

EID: 84899009251     PISSN: 00221503     EISSN: 14657333     Source Type: Journal    
DOI: 10.1093/jhered/esu002     Document Type: Article

References (64)

1. Agui rre JD, Marshall DJ. 2012. Does genetic diversity reduce sibling competition Evolution. 66:94.
2. Ambrogio O, Pechenik J. 2008. When is a male not a male Sex recognition and choice in two sex-changing species. Behav Ecol Sociobiol. 62:1779-1786.
3. Baur B. 1998. Sperm competition in molluscs. In Birkhead TR, Møller AP, editors. Sperm competition and sexual selection. London: Academic Press. p. 255-305.
4. Brante A, Fernà ndez M, Viard F. 2011. Microsatellite evidence for sperm storage and multiple paternity in the marine gastropod Crepidula coquimbensis. J Exp Mar Biol Ecol. 396:83-88.
5. Brante A, Fernández M, Viard F. (2013). Non-random sibling cannibalism in the marine gastropod Crepidula coquimbensis. PLoS ONE. 8:e67050.
6. Brante A, Vilches C, Quin ones A. 2012. Role of population traits and local social interactions in sex-change plasticity of the protandric marine gastropod Crepidula coquimbensis. Mar Ecol Prog Ser. 458:123-132.
7. Brown DI Olivares CA 1996 A new species of Crepidu la (Mollusca: Mesogastropoda: Calyptraeidae) from Chile: additional characters for the identification of eastern Pacific planar Crepidula group J Nat Hist 30 1443-1458.
8. Charnov EL, Bull J. 1977. When is sex environmentally determined Nature. 266:828-830.
9. Coe WR. 1938. Conditions influencing change of sex in mollusks of the genus Crepidula. J Exp Zool. 77:401-424.
10. Collin R. 1995. Se x, size, and position: a test of models predicting size at sex change in the protandrous gastropod Crepidula fornicata. Am Nat. 146:815-831.
11. Collin R. 2001. The effects of mode of development on phylogeography and population structure of North Atlantic Crepidula (Gastropoda: Calyptraeidae). Mol Ecol. 10:2249-2262.
12. Collin R. 2006. Sex ratio, life-history invariants, and patterns of sex change in a family of protandrous gastropods. Evolution. 60:735-745.
13. Daguin-Thiébaut C, Le Cam S, Viard F. 2009. Isolation of 11 microsatellite markers in Crepidula convexa (Gastropoda, Calyptraeideae) for parentage analyses. Mol Ecol Res. 9:917-920.
14. Diaz ER, Thiel M. 2004. Chemical and visual communication during mate searching in rock shrimp. Biol Bull. 206:134-143.
15. Dupont L, Jollivet D, Viard F. 2003. High genetic diversity and ephemeral drift effects in a successful introduced mollusc (Crepidula fornicata: Gastropoda). Mar. Ecol. Prog. Ser. 253:183-195.
16. Dupont L, Richard J, Paulet YM, Thouzeau G, Viard F. 2006. Gregariousness and protandry promote reproductive insurance in the invasive gastropod Crepidula fornicata: evidence from assignment of larval paternity. Mol Ecol. 15:3009-3021.
17. El Mousadik A, Petit RJ. 1996. High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor Appl Genet. 92:832-839.
18. Evans JP, Marshall D. 2005. Male-by-female interactions influence fertilization success and mediate the benefits of polyandry in the sea urchin Heliocidaris erythrograma. Evolution. 59:106-112.
19. Ferdinando B. 1994. Fluctuations and variations in coastal marine environments. Mar Ecol. 15:3-25.
20. Fretter V, Graham A. 1981. The Prosobranch molluscs of Britain and Denmark. Part 6. J Moll Stud. 9:285-363.
21. Gaffney PM, McGee B. 1992. Multiple paternity in Crepidula fornicata (Linnaeus). Veliger. 35:12-15.
22. Ghiselin MT. 1969. The evolution of hermaphroditism among animals. Q Rev Biol. 44:189-208.
23. Giese AC, Pearse JS. 1974. Introduction: general principles. In Giese AC, Pearse JS, editors. Reproduction of marine invertebrates. Vol. 1. New York: Academic Press. p. 1-49.
24. Gosselin T, Sainte-Marie B, Bernatchez L. 2005. Geographic variation of multiple paternity in the American lobster, Homarus americanus. Mol Ecol. 14:1517-1525.
25. Goudet J. 2001. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from: http://www.unil.ch/izea/ softwares/fstat.html. Updated from Goudet (1995).
26. Hendler G, Franz DR. 1971. Population dynamics and life history of Crepriducla convexa say (Gastropoda: Posobranchia) in Delaware Bay. Biol Bull. 141:514-526.
27. Higuchi R. 1989. Rapid, efficient DNA extraction for PCR from cells or blood. Amplifications. 2:1-3.
28. Hoagland KE 1978 Protandry and the evolution of environmentally-mediated sex change: a study of the Mollusca Malacologia 17 365-391.
29. Hoagland KE. 1986. Patterns of encapsulation and brooding in the Calyptraeidae (Prosobranchia: Mesogastropoda). Am Malacol Bull. 4:173-183.
30. Jennions MD, Petrie M. 2000. Why do females mate multiply A review of the genetic benefits. Biol Rev. 75:21-64.
31. Johnson SL, Yund PO. 2007. Variation in multiple paternity in natural populations of a free-spawning marine invertebrate. Mol Ecol. 16:3253-3262.
32. Jones AG. 2001. gerud1.0: a computer program for the reconstruction of parental genotypes from progeny arrays using multilocus DNA data. Mol Ecol Notes. 1:215-218.
33. Kamel SJ, Grosberg RK. 2012. Exclusive male care despite extreme female promiscuity and low paternity in a marine snail. Ecol Lett. 15:1167-1173.
34. Kelly MW, Grosberg RK, Sanford E. 2012. Love the one you're with: proximity determines paternity success in the barnacle Tetraclita rubescens. Mol Ecol. 21:5088-5097.
35. Le Cam S. 2009. Grégarité, changement de sexe et polyandrie: modalitéde la reproduction chez une espèce invasive Crepidula fornicata. Paris: UniversitéPierre et Marie Curie. 250 p.
36. Le Cam S, Pechenik JA, Cagnon M, Viard F. 2009. Fast vs. slow larval growth in an invasive marine mollusc: does paternity matter J Hered. 100:455-464.
37. Levin LA, Bridges TS. 1995. Pattern and diversity in reproduction and development. In McEdward L, editor. Ecology of marine invertebrate larvae. Boca Raton (FL): CRC Press. p. 1-48.
38. Li W, Pechenik JA. 2004. A forced association between the slippersnail Crepidula convexa and the hermit crab Pagurus longicarpus-possible influence from a third party. J Exp Mar Biol Ecol. 311:339-35 4.
39. Li W, Pechenik JA. 2007. Effect of inbreeding on reproduction and juvenile performance in two marine gastropods with contrasting reproductive patterns. Mar Ecol Prog Ser. 346:219-234.
40. Makinen T, Panova M, Andre C. 2007. High levels of multiple paternity in Littorina saxatilis: hedging the bets J Hered. 98:705-711.
41. Marshall DJ, Evans JP. 2007. Context-dependent genetic benefits of polyandry in a marine hermaphrodite. Biol Lett. 3:685-688.
42. McLeod L, Marshall DJ. 2009. Do genetic diversity effects drive the benefits associated with multiple mating A test in a marine invertebrate. PLoS ONE. 4:e6347.
43. Munoz RC, Warner RR. 2003. A new version of the size-advantage hypothesis for sex change: incorporating sperm competition and size-fecundity skew. Am Nat. 161:749-761.
44. Munoz RC, Warner RR. 2004. Testing a new version of the size-advantage hypothesis for sex change: sperm competition and size-skew effects in the bucktooth parrotfish, Sparisoma radians. Behav Biol. 15:129-136.
45. Neff BD, Pitcher TE. 2005. Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol Ecol. 14:19-38.
46. Palmer AR. 1981. Do carbonate skeletons limit the rate of body growth Nature. 292:150-152.
47. Panova M, Boström J, Hofving T, Areskoug T, Eriksson A, Mehlig B, Mäkinen T, AndréC, Johannesson K. 2010. Extreme female promiscuity in a non-social invertebrate species. PLoS ONE. 5:e9640.
48. Paterson IG, Partridge V, Buckland-Nicks J. 2001. Multiple paternity in Littorina obtusata (Gastropoda, Littorinidea) revealed by microsatellite analyses. Biol Bull. 200:261-267.
49. Pawlik JR, Butman CA, Starczak VR. 1991. Hydrodynamic facilitation of gregarious settlement of a reef-building tube worm. Science. 251:421-424.
50. Pearse DE, Janzen FJ, Avise JC. 2001. Genetic markers substantiate long-term storage and utilization of sperm by female painted turtles. Heredity. 86:378-384.
51. Pechenik JA. 1984. The relationship between temperature, growth-rate, and duration of planktonic life for larvae of the gastropod Crepidula fornicata (L). J Exp Mar Biol Ecol. 74:241-257.
52. Proestou DA, Goldsmith MR, Twombly S. 2008. Patterns of male reproductive success in Crepidula fornicata provide new insight for sex allocation and optimal sex change. Biol Bull. 214:194-202.
53. Raymond M, Rousset F. 2003. GENEPOP 3.4., an updated version of GENEPOP V.1.2 (1995): population genetics software for exact tests and ecumenicism. J Hered. 86:248-249.
54. Shaw PW, Sauer WHH. 2004. Multiple paternity and complex fertilisation dynamics in the squid Loligo vulgaris reynaudii. Mar Ecol Prog Ser. 270:173-179.
55. Simmons LW. 2005. The evolution of polyandry: sperm competition, sperm selection, and offspring viability. Annu Rev Ecol Evol Syst. 36:125-146.
56. Sprenger D, Anthes N, Michiels NK. 2008. Multiple mating affects offspring size in the opistobranch Chelidonura sandrana. Mar Biol. 153:891-897.
57. Toonen RJ. 2004. Genetic evidence of multiple paternity of broods in the intertidal crab Petrolisthes cinctipes. Mar Ecol Prog Ser. 270:259-263.
58. Uller T, Olsson M. 2008. Multiple paternity in reptiles: patterns and processes. Mol Ecol. 17:2566-2580.
59. Walker D, Power A, Sweeney-Reeves M, Avise J. 2007. Multiple paternity and female sperm usage along egg-case strings of the knobbed whelk, Busycon carica (Mollusca; Melongenidae). Mar Biol. 151:53-61.
60. Walne PR. 1956. The biology and distribution of the slipper limpet (Crepidula fornicata) in Essex rivers: with notes on the distribution of the larger epibenthi c invertebrates. Fish Invest Ser II. 20:1-50.
61. Wang J. 2004. Sibship reconstruction from genetic data with typing errors. Genetics. 166:1963-1979.
62. Weir BS, Cockerham CC. 1984. Estimating F-statistics for the analysis of population structure. Evolution. 38:1358-1370.
63. Worcester SE. 1994. Adult rafting versus larval swimming: dispersal and recruitment of a botryllid ascidian on eelgrass. Mar Biol. 121:309-317.
64. Yasui Y. 1998. The 'genetic benefits'of female multiple mating reconsidered. Trends Ecol Evol. 13:246-250.