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.
Similar content being viewed by others
References
Allsop DJ, West SA (2003a) Changing sex at the same relative body size. Nature 425:783–784
Allsop DJ, West SA (2003b) Constant relative age and size at sex change for sequentially hermaphroditic fishes. J Evol Biol 16:921–929
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 102:1–13
Antle CE, Klimko L, Harkness W (1970) Confidence intervals for parameters of the logistic distribution. Biometrika 57:397–402
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 561–604
Buston PM, Munday PL, Warner RR (2004) Sex change and relative body size in animals. Nature 428(6983):U1
Charnov EL (1993) Life history invariants. Oxford University Press, Oxford
Charnov EL, Skúladóttir U (2000) Dimensionless invariants for the optimal size (age) of sex change. Evol Ecol Res 2:1067–1071
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 140:337–342
Choat JH, Axe LM, Lou DC (1996) Growth and longevity in fishes of the family Scaridae. Mar Ecol Prog Ser 145(1–3):33–41
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 318:237–246
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 18:1613–1618
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):39–46
Collin R (2006) Sex ratio, life-history invariants, and patterns of sex change in a family of protandrous gastropods. Evolution 60(4):735–745
Crossman DJ, Choat JH, Clements KD et al (2001) Detritus as food for grazing fishes on coral reefs. Limnol Oceanogr 46(7):1596–1605
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 297:259–271
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):79–92
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):551–566
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 13:187–193
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):295–307
Ghiselin MT (1969) The evolution of hermaphroditism among animals. Q Rev Biol 44:189–208
Gust N, Choat JH, Ackerman JL (2002) Demographic plasticity in tropical reef fishes. Mar Biol 140(5):1039–1051
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):2268–2280
Heubel KU, Lindstrom K, Kokko H (2008) Females increase current reproductive effort when future access to males is uncertain. Biol Lett 4(2):224–227
Jones GP (1980) Growth and reproduction in the protogynous hermaphrodite Pseudolabrus celidotus (Pisces: Labridae) in New Zealand. Copeia 1980(4):660–675
Leigh EGJ, Charnov EL, Warner RR (1976) Sex ratio, sex change and natural selection. Proc Natl Acad Sci USA 73(10):3656–3660
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):914–917
Mackie M (2003) Socially controlled sex-change in the half-moon grouper, Epinephelus rivulatus, at Ningaloo Reef, Western Australia. Coral Reefs 22:133–142
Molloy PP, Goodwin NB, Côté IM et al (2007) Predicting the effects of exploitation on male-first sex-changing fish. Anim Conserv 10(1):30–38
Munday PL, Hodges AL, Choat JH et al (2004) Sex-specific growth effects in protogynous hermaphrodites. Can J Fish Aquat Sci 16:323–327
Munday PL, Buston PM, Warner RR (2006) Diversity and flexibility of sex-change strategies in animals. Trends Ecol Evol 21(2):89–95
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):749–761
Nee S, Colegrave N, West SA et al (2005) The illusion of invariant quantities in life histories. Science 309:1236–1239
Nemtzov SC (1985) Social control of sex change in the Red Sea razorfish Xyrichthys pentadactylus (Teleosteii, Labridae). Environ Biol Fishes 14(2–3):199–211
Paddack MJ (2005) Herbivorous coral reef fishes in a changing ecosystem. PhD Dissertation, University of Miami
Paddack MJ, Sponaugle S, Cowen RK (2009) Small-scale demographic variation in the stoplight parrotfish Sparisoma viride. J Fish Biol 75:2509–2526
Policansky D (1982) Sex change in plants and animals. Annu Rev Ecol Syst 13:471–495
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 13:109–119
Robertson DR, Warner RR (1978) Sexual patterns in the labroid fishes of the western Caribbean, II: the parrotfish (Scaridae). Smithson Contrib Zool 255:1–26
Schafer RE, Sheffield TS (1973) Inferences on the parameters of the logistic distribution. Biometrics 29(3):449–455
Shapiro DY (1981) Size, maturation and the social control of sex reversal in the coral reef fish Anthias squamipinnis. J Zool 193:105–128
van Rooij JM, Videler JJ (1997) Mortality estimates from repeated visual censuses of a parrotfish (Sparisoma viridae) population: demographic implications. Mar Biol 128:385–396
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 122:93–105
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 209–245
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 266:201–212
Warner RR (1975) The adaptive significance of sequential hermaphroditism in animals. Am Nat 109:61–82
Warner RR, Swearer SE (1991) Social control of sex change in Bluehead wrasse, Thalassoma bifasciatum (Pisces: Labridae). Biol Bull 181:199–294
Warton DI, Wright IJ, Falster DS et al (2006) Bivariate line-fitting methods for allometry. Biol Rev Camb Philos Soc 81:259–291
Westneat MW, Alfaro ME (2005) Phylogenetic relationships and evolutionary history of the reef fish family Labridae. Mol Phylogen Evol 36:370–390
Zar JH (1999) Biostatistical analysis. Prentice Hall, Englewood Cliffs
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Molloy, P.P., Paddack, M.J., Reynolds, J.D. et al. Relative size-at-sex-change in parrotfishes across the Caribbean: is there variance in a supposed life-history invariant?. Evol Ecol 25, 429–446 (2011). https://doi.org/10.1007/s10682-010-9404-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10682-010-9404-3