Skip to main content
Log in

Do sex-changing male snails use mate choice to get a jump on their “size advantage”?

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Individuals of species that change sex from male to female may gain a “size advantage” from that sex change; that is, as males become larger, they become female, thus increasing their fecundity with their size. However, males could also gain an early and different reproductive size advantage by choosing large females as mates. While male preference for large females has been observed in many dioecious species, we know little about male size preference in sex-changing species. In choice experiments, we examined whether males of two congeneric species of marine sex-changing snails, Crepidula fornicata and C. convexa, chose large females over small ones as partners. We also used choice tests to see whether males of C. fornicata, a species whose members form long-term, multi-animal stacks, would choose two females in a stack over a single female. Surprisingly, males of neither species showed a preference for large females, in spite of the documented fecundity advantage associated with large female-size. Males of C. fornicata chose slightly, but not significantly, more single females than stacks, suggesting that neither number nor size drives mate choice in these animals. Key factors that may influence this lack of size preference include long association time, the likelihood of sperm competition, and the cost of extended mate search; it may also be that sex-change itself, the very factor that creates female-biased sexual size dimorphism in these species, prevents size preference, as males may gain sufficient reproductive advantage from eventually becoming large females themselves to offset any benefit of choosing large females.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ambrogio OV, Pechenik JA (2008) When is a male not a male? Sex recognition and choice in two sex-changing species. Behav Ecol Sociobiol 62:1779–1786. doi:10.1007/s00265-008-0606-4

    Article  Google Scholar 

  • Andersson M (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  • Backwell PRY, Passmore NI (1996) Time constraints and multiple choice criteria in the sampling behaviour and mate choice of the fiddler crab, Uca annulipes. Behav Ecol Sociobiol 38:407–416

    Article  Google Scholar 

  • Basolo AL (2004) Variation between and within the sexes in body size preferences. Anim Behav 68:75–82

    Article  Google Scholar 

  • Bateman PW, Fleming PA (2006) Males are selective too: mating, but not courtship, with sequential females influences choosiness in male field crickets (Gryllus bimaculatus). Behav Ecol Sociobiol 59:577–581

    Article  Google Scholar 

  • Bel-Venner MC, Dray S, Allaine D, Menu F, Venner S (2008) Unexpected male choosiness for mates in a spider. Proc R Soc Lond B Biol Sci 275:77–82

    Article  CAS  Google Scholar 

  • Bonduriansky R (2001) The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biol Rev 76:305–339

    Article  PubMed  CAS  Google Scholar 

  • Borg AA, Forsgren E, Amundsen T (2006) Seasonal change in female choice for male size in the two-spotted goby. Anim Behav 72:763–771

    Article  Google Scholar 

  • Cardoso RS, Costa DS, Loureiro VF (2007) Mating behaviour of the marine snail Littoraria flava (Mollusca: Caenogastropoda) on a boulder shore of south-east Brazil. J Mar Biol Assoc UK 87:947–952

    Article  Google Scholar 

  • Coe W (1938a) Conditions influencing the change of sex in mollusks of the genus Crepidula. J Exp Biol 122:5–19

    Google Scholar 

  • Coe W (1938b) Influence of association on the sexual phases of gastropods having protrandric consecutive sexuality. Biol Bull 75:274–285

    Article  Google Scholar 

  • Coe WR (1953) Influences of association, isolation, and nutrition on the sexuality of snails of the genus Crepidula. J Exp Zool 122:5–19

    Article  Google Scholar 

  • Collin R (1995) Sex, size, and position: a test of models predicting size at sex change in the protandrous gastropod Crepidula fornicata. Am Nat 146:815–831

    Article  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Gaffney PM, McGee B (1992) Multiple paternity in Crepidula fornicata (Linnaeus). Veliger 35:12–15

    Google Scholar 

  • Ghiselin M (1969) The evolution of hermaphroditism among animals. Q Rev Biol 44:189–208

    Article  PubMed  CAS  Google Scholar 

  • Gwynne DT (1991) Sexual competition among females––what causes courtship-role reversal? Trends Ecol Evol 6:118–121

    Article  Google Scholar 

  • Hendler G, Franz DR (1971) Population dynamics and life-history of Crepidula convexa Say (Gastropoda-Prosobranchia) in Delaware Bay. Biol Bull 141:514

    Article  Google Scholar 

  • Herdman EJE, Kelly CD, Godin JGJ (2004) Male mate choice in the guppy (Poecilia reticulata): Do males prefer larger females as mates? Ethology 110:97–111

    Article  Google Scholar 

  • Hoagland KE (1978) Protandry and the evolution of environmentally mediated sex change: a study of the Mollusca. Malacologia 176:365–391

    Google Scholar 

  • Hoefler CD (2007) Male mate choice and size-assortative pairing in a jumping spider, Phidippus clarus. Anim Behav 73:943–954

    Article  Google Scholar 

  • Johnson L (1999) Size assortative mating in the marine snail Littorina neglecta. J Exp Mar Biol Ecol 79:1131–1132

    Google Scholar 

  • Lehmann GUC (2007) Density-dependent plasticity of sequential mate choice in a bushcricket (Orthoptera: Tettigoniidae). Aust J Zool 55:123–130

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lynch KS, Rand AS, Ryan MJ, Wilczynski W (2005) Plasticity in female mate choice associated with changing reproductive states. Anim Behav 69:689–699

    Article  Google Scholar 

  • Megina C, Cervera JL (2003) Diet, prey selection and cannibalism in the hunter opisthobranch Roboastra europaea. J Mar Biol Assoc UK 83:489–495

    Article  Google Scholar 

  • Muñoz R, Warner R (2003) A new version of the size-advantage hypothesis for sex change: incorporating sperm competition and size-fecundity skew. Am Nat 161:749–761

    Article  PubMed  Google Scholar 

  • Orton J (1909) On the occurrence of protandric hermaphroditism in the mollusc Crepidula fornicata. Proc Roy Soc London 81:468–484

    Article  Google Scholar 

  • Pechenik JA, Gee CC (1993) Onset of metamorphic competence in larvae of the gastropod Crepidula fornicata (L.), judged by a natural and an artificial cue. J Exp Mar Biol Ecol 167:59–72

    Article  Google Scholar 

  • Poschadel JR, Meyer-Lucht Y, Plath M (2006) Response to chemical cues from conspecifics reflects male mating preference for large females and avoidance of large competitors in the European pond turtle, Emys orbicularis. Behaviour 143:569–587

    Article  Google Scholar 

  • Preston BT, Stevenson IR, Pemberton JM, Coltman DW, Wilson K (2005) Male mate choice influences female promiscuity in Soay sheep. Proc R Soc Lond B Biol Sci 272:365–373

    Article  CAS  Google Scholar 

  • Proestou D, Goldsmith M, Twombly S (2008) Patterns of male reproductive success in Crepidula fornicata provides new insight for sex allocation and optimal sex change. Biol Bull 214:194–202

    Article  PubMed  Google Scholar 

  • Ptacek MB, Travis J (1997) Mate choice in the sailfin molly, Poecilia latipinna. Evol Int J org Evol 51:1217–1231

    Google Scholar 

  • Rahman N, Dunham DW, Govind CK (2002) Size-assortative pairing in the big-clawed snapping shrimp, Alpheus heterochelis. Behaviour 139:1443–1468

    Article  Google Scholar 

  • Reading KL, Backwell PRY (2007) Can beggars be choosers? Male mate choice in a fiddler crab. Anim Behav 74:867–872

    Article  Google Scholar 

  • Shine R, Philips B, Waye H, LeMaster M, Mason R (2003) The lexicon of love: what cues cause size-assortative courtship by male garter snakes? Behav Ecol Sociobiol 53:243–237

    Article  Google Scholar 

  • Shine R, Webb JK, Lane A, Mason RT (2006) Flexible mate choice: a male snake’s preference for larger females is modified by the sizes of females encountered. Anim Behav 71:203–209

    Article  Google Scholar 

  • Warner R, Fitch D, Standish J (1996) Social control of sex change in the shelf limpet Crepidula norrisiarum: size-specific responses to local group composition. J Exp Mar Biol Ecol 204:155–167

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Olivia V. Ambrogio.

Additional information

Communicated by M. Byrne.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ambrogio, O.V., Pechenik, J.A. Do sex-changing male snails use mate choice to get a jump on their “size advantage”?. Mar Biol 156, 2173–2180 (2009). https://doi.org/10.1007/s00227-009-1247-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-009-1247-5

Keywords

Navigation