Marine Biology

, Volume 148, Issue 1, pp 213–221 | Cite as

Cuckoldry rates in the Molly Miller (scartella cristata; blenniidae), a hole-nesting marine fish with alternative reproductive tactics

  • Mark MackiewiczEmail author
  • Brady A. Porter
  • Elizabeth E. Dakin
  • John C. Avise
Research Article


Microsatellite markers were developed and employed to assess genetic maternity and paternity of embryos in nest-tended clutches of the Molly Miller (Scartella cristata), a marine fish in which alternative reproductive tactics (ARTs) by males were recently described from behavioral and morphological evidence. Genetic data gathered for 1,536 surveyed progeny, from 23 barnacle-nest holes in a single Floridian population, indicate that on average about 5.5 females (range 3–9) contributed to the pool of progeny within a nest. With regard to paternity, the microsatellite data demonstrate that most of the surveyed nests (82.6%) contained at least some embryos that had not been sired by the nest-tending (bourgeois) male, and overall that 12.4% of offspring in the population had been sired via "stolen" fertilizations by other males. These are among the highest values of cuckoldry documented to date in nest-tending fishes, and they support and quantify the notion that the nest-parasitic ART is reproductively quite successful in this species despite what would otherwise seem to be highly defensible nesting sites (the restricted interior space of a barnacle shell). Our estimated cuckoldry rates in this population of the Molly Miller are compared to those previously reported for local populations in other nest-tending fish species, with results discussed in the context of ecological and behavioral variables that may influence relative frequencies of nest parasitism.


Parasitic Male Exclusion Probability Sand Goby Typical Nest Nest Parasitism 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank Judith Mank and DeEtte Walker for useful comments on the manuscript. We are grateful to John Barnes, Joe Nairn, and Travis Glenn for suggestions in preparing the genomic library and in microsatellite isolation. Work was carried out at the Genome Analysis Facility at the University of Georgia, and was supported by University funds and by a Pew Foundation fellowship (to John C. Avise). All experiments were performed in the United States and comply with the laws therein.


  1. Avise JC, Jones AG, Walker D, DeWoody JA (2002) Genetic mating systems and reproductive natural histories of fishes: lessons for ecology and evolution. Annu Rev Genet 36:19–45CrossRefGoogle Scholar
  2. Boutin-Ganache I, Raposo M, Raymond M, Deschepper CF (2001) M13-tailed primers improve the readability and usability of microsatellite analyses performed with two different allele-sizing methods. Biotechniques 31:24–28CrossRefGoogle Scholar
  3. Croshaw DA, Glenn TC (2003) Seven polymorphic microsatellite DNA loci from the red-spotted newt (Notophthalmus viridescens). Mol Ecol Notes 3:514–516CrossRefGoogle Scholar
  4. DeWoody JA, Avise JC (2001) Genetic perspectives on the natural history of fish mating systems. J Hered 92:167–172CrossRefGoogle Scholar
  5. DeWoody JA, Fletcher DE, Wilkins SD, Nelson WS, Avise JC (1998) Molecular genetic dissection of spawning, parentage, and reproductive tactics in a population of redbreast sunfish, Lepomis auritus. Evolution 52:1802–1810CrossRefGoogle Scholar
  6. Dewoody JA, Dewoody YD, Fiumera AC, Avise JC (2000) On the number of reproductives contributing to a half-sib progeny array. Genet Res 75:95–105CrossRefGoogle Scholar
  7. DeWoody JA, Fletcher DE, Mackiewicz M, Wilkins SD, Avise JC (2000a) The genetic mating system of spotted sunfish (Lepomis punctatus): mate numbers and the influence of male reproductive parasites. Mol Ecol 9:2119–2128CrossRefGoogle Scholar
  8. DeWoody JA, Fletcher DE, Wilkins SD, Avise JC (2000b) Parentage and nest guarding in the Tessellated Darter (Etheostoma olmstedi) assayed by microsatellite markers (Perciformes: Percidae). Copeia 2000:740–747CrossRefGoogle Scholar
  9. DeWoody JA, Fletcher DE, Wilkins SD, Nelson WS, Avise JC (2000c) Genetic monogamy and biparental care in an externally fertilizing fish, the largemouth bass (Micropterus salmoides). Proc R Soc Lond Ser B 267:2431–2437CrossRefGoogle Scholar
  10. Fiumera AC, Porter BA, Grossman GD, and Avise JC (2002) Intensive genetic assessment of the mating system and reproductive success in a semi-closed population of the mottled sculpin, Cottus bairdi. Mol Ecol 11:2367–2377CrossRefGoogle Scholar
  11. Gilbert CR (2002) National Audubon society field fuide to fishes (North America). Alfred A Knopf, New YorkGoogle Scholar
  12. Goncalves D, Fagundes T, Oliveira R (2003a) Reproductive behaviour of sneaker males of the peacock blenny. J Fish Biol 63:528–532CrossRefGoogle Scholar
  13. Goncalves D, Oliveira RF, Korner K, Schlupp I (2003b) Intersexual copying by sneaker males of the peacock blenny. Anim Behav 65:355–361CrossRefGoogle Scholar
  14. Gross MR (1979) Cuckoldry in sunfishes (Lepomis; Centrarchidae). Can J Zool 57:1507–1509CrossRefGoogle Scholar
  15. Gross MR (1982) Sneakers, satellites and parentals—polymorphic mating strategies in North American sunfishes. J Comp Ethol 60:1–26Google Scholar
  16. Gross MR (1991) Evolution of alternative reproductive strategies– Frequency-dependent sexual selection in male bluegill sunfish. Philos Trans R Soc Lond Ser B 332:59–66CrossRefGoogle Scholar
  17. Gross MR (1996) Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol Evol 11:A92–A98CrossRefGoogle Scholar
  18. Gross MR, Charnov EL (1980) Alternative male life histories in bluegill sunfish. Proc Natl Acad Sci USA 77:6937–6940CrossRefGoogle Scholar
  19. Gross MR, Macmillan AM (1981) Predation and the evolution of colonial nesting in bluegill sunfish (Lepomis macrochirus). Behav Ecol Sociobiol 8:163–174CrossRefGoogle Scholar
  20. Gross MR, Shine R (1981) Parental care and mode of fertilization in ectothermic vertebrates. Evolution 35:775–793CrossRefGoogle Scholar
  21. Hamilton MB, Pincus EL, Di Fiore A, Flescher RC (1999) Universal linker and ligation procedures for construction of genomic DNA libraries enriched for microsatellites. Biotechniques 27:500–507CrossRefGoogle Scholar
  22. Hauswaldt JS, Glenn TC (2003) Microsatellite DNA loci from the diamondback terrapin (Malaclemys terrapin). Mol Ecol Notes 3:174–176CrossRefGoogle Scholar
  23. Jones AG, Avise JC (1997) Polygynandry in the dusky pipefish (Syngnathus floridae) revealed by microsatellite DNA markers. Evolution 51:1611–1622CrossRefGoogle Scholar
  24. Jones AG, Avise JC (2001) Mating systems and sexual selection in male-pregnant pipefishes and seahorses: insights from microsatellite-based studies of maternity. J Hered 92:150–158CrossRefGoogle Scholar
  25. Jones AG, Ostlund-Nilsson S, Avise JC (1998) A microsatellite assessment of sneaked fertilizations and egg thievery in the fifteenspine stickleback. Evolution 52:848–858CrossRefGoogle Scholar
  26. Jones AG, Walker D, Kvarnemo C, Lindstrom K, Avise JC (2001a) How cuckoldry can decrease the opportunity for sexual selection: data and theory from a genetic parentage analysis of the sand goby, Pomatoschistus minutus. Proc Natl Acad Sci USA 98:9151–9156CrossRefGoogle Scholar
  27. Jones AG, Walker D, Lindstrom K, Kvarnemo C, Avise JC (2001b) Surprising similarity of sneaking rates and genetic mating patterns in two populations of sand goby experiencing disparate sexual selection regimes. Mol Ecol 10:461–469CrossRefGoogle Scholar
  28. Kellogg KA, Markert JA, Stauffer JR, Kocher TD (1998) Intraspecific brood mixing and reduced polyandry in a maternal mouth-brooding cichlid. Behav Ecol 9:309–312CrossRefGoogle Scholar
  29. Mackiewicz M, Fletcher DE, Wilkins SD, DeWoody JA, Avise JC (2002) A genetic assessment of parentage in a natural population of dollar sunfish (Lepomis marginatus) based on microsatellite markers. Mol Ecol 11:1877–1883CrossRefGoogle Scholar
  30. McCoy EE, Jones AG, Avise JC (2001) The genetic mating system and tests for cuckoldry in a pipefish species in which males fertilize eggs and brood offspring externally. Mol Ecol 10:1793–1800CrossRefGoogle Scholar
  31. McEachran JD (1998) Fishes of the Gulf of Mexico. University of Texas Press, AustinGoogle Scholar
  32. Miranda JA, Oliveira RF, Carneiro LA, Santos RS, Grober MS (2003) Neurochemical correlates of male polymorphism and alternative reproductive tactics in the Azorean rock-pool blenny, Parablennius parvicornis. Gen Comp Endocrinol 132:183–189CrossRefGoogle Scholar
  33. Neat FC (2001) Male parasitic spawning in two species of triplefin blenny (Tripterigiidae): contrasts in demography, behaviour and gonadal characteristics. Environ Biol Fishes 61:57–64CrossRefGoogle Scholar
  34. Neat FC, Locatello L (2002) No reason to sneak: why males of all sizes can breed in the hole nesting blenny, Aidablennius sphinx. Behav Ecol Sociobiol 52:66–73CrossRefGoogle Scholar
  35. Neat FC, Locatello L, Rasotto MB (2003) Reproductive morphology in relation to alternative male reproductive tactics in Scartella cristata. J Fish Biol 62:1381–1391CrossRefGoogle Scholar
  36. Neff BD (2001) Genetic paternity analysis and breeding success in bluegill sunfish (Lepomis macrochiros). J Hered 92:111–119CrossRefGoogle Scholar
  37. Oliveira RF, Miranda JA, Carvalho N, et al. (2000) Male mating success in the Azorean rock pool blenny:the effects of body size, male behaviour and nest characteristics. J Fish Biol 57:1416–1428CrossRefGoogle Scholar
  38. Oliveira RF, Canario AVM, Grober MS (2001a) Male sexual polymorphism, alternative reproductive tactics, and androgens in combtooth blennies (Pisces: Blenniidae). Horm Behav 40:266–275CrossRefGoogle Scholar
  39. Oliveira RF, Goncalves EJ, Santos RS (2001b) Gonadal investment of young males in two blenniid fishes with alternative mating tactics. J Fish Biol 59:459–462CrossRefGoogle Scholar
  40. Oliveira RF, Carvalho N, Miranda J, et al. (2002) The relationship between the presence of satellite males and nest© holders’mating success in the Azorean rock-pool blenny, Parablennius sanguinolentus parvicornis. Ethology 108:223–235CrossRefGoogle Scholar
  41. Philipp DP, Gross MR (1994) Genetic evidence for cuckoldry in bluegill, Lepomis macrochirus. Mol Ecol 3:563–569CrossRefGoogle Scholar
  42. Porter BA, Fiumera AC, Avise JC (2002) Egg mimicry and allopaternal care:two mate attracting tactics by which nesting striped darter (Etheostoma virgatum) males enhance reproductive success. Behav Ecol Sociobiol 51:350–359CrossRefGoogle Scholar
  43. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249CrossRefGoogle Scholar
  44. Robins RC (1986) A field guide to Atlantic coast fishes of North America. Houghton Mifflin, BostonGoogle Scholar
  45. Selvin S (1980) Probability of nonpaternity determined by multiple allele codominant systems. Am J Hum Genet 32:276–278PubMedPubMedCentralGoogle Scholar
  46. Taborsky M (1994) Sneakers, satellites, and helpers—parasitic and cooperative behavior in fish reproduction. Adv Study Behav 23:1–100CrossRefGoogle Scholar
  47. Taborsky M (1997) Bourgeois and parasitic tactics: do we need collective, functional terms for alternative reproductive behaviours? Behav Ecol Sociobiol 41:361–362CrossRefGoogle Scholar
  48. Taborsky M (1998) Sperm competition in fish: ’bourgeois’ males and parasitic spawning. Trends Ecol Evol 13:222–227CrossRefGoogle Scholar
  49. Taborsky M (2001) The evolution of bourgeois, parasitic, and cooperative reproductive behaviors in fishes. J Hered 92:100–110CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Mark Mackiewicz
    • 1
    Email author
  • Brady A. Porter
    • 2
  • Elizabeth E. Dakin
    • 1
  • John C. Avise
    • 1
  1. 1.Department of GeneticsUniversity of GeorgiaAthensUSA
  2. 2.Department of Biological SciencesDuquesne UniversityPittsburghUSA

Personalised recommendations