Advertisement

Evolutionary Ecology

, Volume 25, Issue 2, pp 429–446 | Cite as

Relative size-at-sex-change in parrotfishes across the Caribbean: is there variance in a supposed life-history invariant?

  • Philip P. Molloy
  • Michelle J. Paddack
  • John D. Reynolds
  • Matthew J. G. Gage
  • Isabelle M. Côté
Research Article

Abstract

Invariant life-history theory has been used to identify parallels in life histories across diverse taxa. One important invariant life-history model predicts that, given simple assumptions and conditions, size-at-sex-change relative to maximum attainable body size (relative size-at-sex-change, RSSC) will be invariant across populations and species in sequential hermaphrodites. Even if there are broad species-wide limits to RSSC, populations could fine-tune RSSC to local conditions and, consequently, exhibit subtle but important differences in timing of sex change. Previous analyses of the invariant sex-change model have not explicitly considered the potential for meaningful differences in RSSC within the confines of a broader ‘invariance’. Furthermore, these tests differ in their geographical and taxonomic scope, which could account for their conflicting conclusions. We test the model using several populations of three female-first sex-changing Caribbean parrotfish species. We first test for species-wide invariance using traditional log–log regressions and randomisation analyses of population-specific point estimates of RSSC. We then consider error around these point estimates, which is rarely incorporated into invariant analyses, to test for differences among populations in RSSC. Log–log regressions could not unequivocally diagnose invariance in RSSC across populations; randomisation tests identified an invariant RSSC in redband parrotfish only. Analyses that incorporated within-population variability in RSSC revealed differences among populations in timing of sex change, which were independent of geography for all species. While RSSC may be evolutionarily constrained (as in redband parrotfish), within these bounds the timing of sex change may vary among populations. This variability is overlooked by traditional invariant analyses and not predicted by the existing invariant model.

Keywords

Hermaphroditism Invariant life-history analysis Protandry Protogyny Sex allocation theory Sex change 

Notes

Acknowledgments

Thanks to Fab* and Earth2Ocean labs at Simon Fraser University, Jenn Sunday, Maria José Juan Jorda, Arne Mooers, Wendy Palen, Nick Dulvy, Stuart West, Nick Colegrave, Wolf Blanckenhorn, Martin Reichard and two anonymous reviewers for helpful feedback on earlier versions of this manuscript, Alex Chubaty for help with R coding, and Marianne Fish for help creating Fig. 2. Particular thanks to Pete Buston for his suggestions regarding the framework of this manuscript, Table 1 and other useful comments. This is a contribution from the Earth2Ocean Group and Project Seahorse. P.P.M. was supported by the John and Pamela Salter Charitable Trust, a BBSRC studentship 02/A1/S/08113, a Leverhulme studentship # SAS/30146, a Government of Canada post-doctoral research fellowship and Conservation International’s Marine Management Area Science program. M.J.P. was supported by the National Center for Caribbean Coral Reef Research (NCORE) through EPA grant #R828020. I.M.C. and J.D.R. were supported by NSERC of Canada Discovery Grants.

References

  1. Allsop DJ, West SA (2003a) Changing sex at the same relative body size. Nature 425:783–784CrossRefPubMedGoogle Scholar
  2. Allsop DJ, West SA (2003b) Constant relative age and size at sex change for sequentially hermaphroditic fishes. J Evol Biol 16:921–929CrossRefPubMedGoogle Scholar
  3. Alonzo SH, Mangel M (2004) The effects of size-selective fisheries on the stock dynamics of and sperm limitation in sex-changing fish. Fish Bull 102:1–13Google Scholar
  4. Antle CE, Klimko L, Harkness W (1970) Confidence intervals for parameters of the logistic distribution. Biometrika 57:397–402CrossRefGoogle Scholar
  5. Bannerot S, Fox WWJ, Powers JE (1987) Reproductive strategies and the management of snappers and groupers in the Gulf of Mexico and Caribbean. In: Polovina JJ, Ralston S (eds) Tropical snappers and groupers: biology and fisheries management. Westview Press, Boulder, pp 561–604Google Scholar
  6. Buston PM, Munday PL, Warner RR (2004) Sex change and relative body size in animals. Nature 428(6983):U1CrossRefGoogle Scholar
  7. Charnov EL (1993) Life history invariants. Oxford University Press, OxfordGoogle Scholar
  8. Charnov EL, Skúladóttir U (2000) Dimensionless invariants for the optimal size (age) of sex change. Evol Ecol Res 2:1067–1071Google Scholar
  9. Chen M-H, Soong K (2002) Estimation of age in the sex-changing, coral-inhibiting snail Coralliophila violacea from growth striae and a mark-recapture experiment. Mar Biol 140:337–342CrossRefGoogle Scholar
  10. Choat JH, Axe LM, Lou DC (1996) Growth and longevity in fishes of the family Scaridae. Mar Ecol Prog Ser 145(1–3):33–41CrossRefGoogle Scholar
  11. Choat JH, Davies CR, Ackerman JL et al (2006) Age structure and growth in a large teleost, Cheilinus undulatus, with a review of size distribution in labrid fishes. Mar Ecol Prog Ser 318:237–246CrossRefGoogle Scholar
  12. Cipriani R, Collin R (2005) Life-history invariants with bounded variables cannot be distinguish from data generated by random processes using standard analyses. J Evol Biol 18:1613–1618CrossRefPubMedGoogle Scholar
  13. Clifton KE (1995) Asynchronous food availability on neighboring Caribbean coral reefs determines seasonal patterns of growth and reproduction for the herbivorous parrotfish Scarus iserti. Mar Ecol Prog Ser 116(1):39–46CrossRefGoogle Scholar
  14. Collin R (2006) Sex ratio, life-history invariants, and patterns of sex change in a family of protandrous gastropods. Evolution 60(4):735–745PubMedGoogle Scholar
  15. Crossman DJ, Choat JH, Clements KD et al (2001) Detritus as food for grazing fishes on coral reefs. Limnol Oceanogr 46(7):1596–1605CrossRefGoogle Scholar
  16. DeMartini EE, Friedlander A, Holzwarth SR (2005) Size at sex change in protogynous labroids, prey body size distributions, and apex predator densities at NW Hawaiin atolls. Mar Ecol Prog Ser 297:259–271CrossRefGoogle Scholar
  17. Fairhurst L, Attwood CG, Durholtz MD et al (2007) Life history of the steentjie Spondyliosoma emarginatum (Cuvier 1830) in Langebaan Lagoon, South Africa. Afr J Mar Sci 29(1):79–92CrossRefGoogle Scholar
  18. Gardner A, Allsop DJ, Charnov EL et al (2005) A dimensionless invariant for relative size at sex change in animals: explanations and implications. Am Nat 165(5):551–566CrossRefPubMedGoogle Scholar
  19. Garratt PA, Govender A, Punt AE (1993) Growth acceleration at sex change in the protogynous hermaphrodite Chrysoblephus puniceus (Pisces: Sparidae). S Afr J Mar Sci 13:187–193Google Scholar
  20. Gavio MA, Orensanz JML, Armstrong D (2006) Evaluation of alternative life history hypotheses for the sand shrimp Crangon franciscorum (Decapoda: Caridea). J Crust Biol 26(3):295–307CrossRefGoogle Scholar
  21. Ghiselin MT (1969) The evolution of hermaphroditism among animals. Q Rev Biol 44:189–208CrossRefPubMedGoogle Scholar
  22. Gust N, Choat JH, Ackerman JL (2002) Demographic plasticity in tropical reef fishes. Mar Biol 140(5):1039–1051CrossRefGoogle Scholar
  23. Hamilton SL, Caselle JE, Standish JD et al (2007) Size-selective harvesting alters life histories of a temperate sex-changing fish. Ecol Appl 17(8):2268–2280CrossRefPubMedGoogle Scholar
  24. Heubel KU, Lindstrom K, Kokko H (2008) Females increase current reproductive effort when future access to males is uncertain. Biol Lett 4(2):224–227CrossRefPubMedGoogle Scholar
  25. Jones GP (1980) Growth and reproduction in the protogynous hermaphrodite Pseudolabrus celidotus (Pisces: Labridae) in New Zealand. Copeia 1980(4):660–675CrossRefGoogle Scholar
  26. Leigh EGJ, Charnov EL, Warner RR (1976) Sex ratio, sex change and natural selection. Proc Natl Acad Sci USA 73(10):3656–3660CrossRefPubMedGoogle Scholar
  27. Linde M, Palmer M (2008) Testing Allsop and West’s size at sex change invariant within a fish species: a spurious ratio or a useful group descriptor? J Evol Biol 21(3):914–917CrossRefPubMedGoogle Scholar
  28. Mackie M (2003) Socially controlled sex-change in the half-moon grouper, Epinephelus rivulatus, at Ningaloo Reef, Western Australia. Coral Reefs 22:133–142CrossRefGoogle Scholar
  29. Molloy PP, Goodwin NB, Côté IM et al (2007) Predicting the effects of exploitation on male-first sex-changing fish. Anim Conserv 10(1):30–38CrossRefGoogle Scholar
  30. Munday PL, Hodges AL, Choat JH et al (2004) Sex-specific growth effects in protogynous hermaphrodites. Can J Fish Aquat Sci 16:323–327CrossRefGoogle Scholar
  31. Munday PL, Buston PM, Warner RR (2006) Diversity and flexibility of sex-change strategies in animals. Trends Ecol Evol 21(2):89–95CrossRefPubMedGoogle Scholar
  32. Muñoz 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(5):749–761CrossRefPubMedGoogle Scholar
  33. Nee S, Colegrave N, West SA et al (2005) The illusion of invariant quantities in life histories. Science 309:1236–1239CrossRefPubMedGoogle Scholar
  34. Nemtzov SC (1985) Social control of sex change in the Red Sea razorfish Xyrichthys pentadactylus (Teleosteii, Labridae). Environ Biol Fishes 14(2–3):199–211CrossRefGoogle Scholar
  35. Paddack MJ (2005) Herbivorous coral reef fishes in a changing ecosystem. PhD Dissertation, University of MiamiGoogle Scholar
  36. Paddack MJ, Sponaugle S, Cowen RK (2009) Small-scale demographic variation in the stoplight parrotfish Sparisoma viride. J Fish Biol 75:2509–2526CrossRefPubMedGoogle Scholar
  37. Policansky D (1982) Sex change in plants and animals. Annu Rev Ecol Syst 13:471–495CrossRefGoogle Scholar
  38. Punt AE, Garratt PA, Govender A (1993) On an approach for applying per-recruit methods to a protogynous hermaphrodite, with an illustration for the slinger Chrysoblephus puniceus (Pisces: Sparidae). Afr J Mar Sci 13:109–119Google Scholar
  39. Robertson DR, Warner RR (1978) Sexual patterns in the labroid fishes of the western Caribbean, II: the parrotfish (Scaridae). Smithson Contrib Zool 255:1–26Google Scholar
  40. Schafer RE, Sheffield TS (1973) Inferences on the parameters of the logistic distribution. Biometrics 29(3):449–455CrossRefGoogle Scholar
  41. Shapiro DY (1981) Size, maturation and the social control of sex reversal in the coral reef fish Anthias squamipinnis. J Zool 193:105–128CrossRefGoogle Scholar
  42. van Rooij JM, Videler JJ (1997) Mortality estimates from repeated visual censuses of a parrotfish (Sparisoma viridae) population: demographic implications. Mar Biol 128:385–396CrossRefGoogle Scholar
  43. van Rooij JM, Bruggemann JH, Videler JJ et al (1995) Plastic growth of the herbivorous reef fish Sparisoma viride: field evidence for a trade-off between growth and reproduction. Mar Ecol Prog Ser 122:93–105CrossRefGoogle Scholar
  44. Vincent ACJ, Sadovy Y (1998) Reproductive ecology and the conservation and management of fishes. In: Caro TM (ed) Behavioral ecology and conservation biology. Oxford University Press, Oxford, pp 209–245Google Scholar
  45. Walker SPW, McCormick MI (2004) Otolith-check formation and accelerated growth associated with sex change in an annual protogynous tropical fish. Mar Ecol Prog Ser 266:201–212CrossRefGoogle Scholar
  46. Warner RR (1975) The adaptive significance of sequential hermaphroditism in animals. Am Nat 109:61–82CrossRefGoogle Scholar
  47. Warner RR, Swearer SE (1991) Social control of sex change in Bluehead wrasse, Thalassoma bifasciatum (Pisces: Labridae). Biol Bull 181:199–294CrossRefGoogle Scholar
  48. Warton DI, Wright IJ, Falster DS et al (2006) Bivariate line-fitting methods for allometry. Biol Rev Camb Philos Soc 81:259–291CrossRefPubMedGoogle Scholar
  49. Westneat MW, Alfaro ME (2005) Phylogenetic relationships and evolutionary history of the reef fish family Labridae. Mol Phylogen Evol 36:370–390CrossRefGoogle Scholar
  50. Zar JH (1999) Biostatistical analysis. Prentice Hall, Englewood CliffsGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Philip P. Molloy
    • 1
    • 2
    • 3
  • Michelle J. Paddack
    • 2
    • 3
    • 4
  • John D. Reynolds
    • 2
  • Matthew J. G. Gage
    • 3
  • Isabelle M. Côté
    • 2
  1. 1.Project SeahorseUniversity of British ColumbiaVancouverCanada
  2. 2.Department of Biological SciencesSimon Fraser UniversityBurnabyCanada
  3. 3.School of Biological SciencesUniversity of East AngliaNorwichUK
  4. 4.Santa Barbara City CollegeSanta BarbaraUSA

Personalised recommendations