Skip to main content
SpringerLink
Log in

Sex-specific responses to fecundity selection in the broad-nosed pipefish

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Fecundity selection, acting on traits enhancing reproductive output, is an important determinant of organismal body size. Due to a unique mode of reproduction, mating success and fecundity are positively correlated with body size in both sexes of male-pregnant Syngnathus pipefish. As male pipefish brood eggs on their tail and egg production in females occurs in their ovaries (located in the trunk region), fecundity selection is expected to affect both sexes in this species, and is predicted to act differently on body proportions of males and females during their development. Based on this hypothesis, we investigated sexual size dimorphism in body size allometry and vertebral numbers across populations of the widespread European pipefish Syngnathus typhle. Despite the absence of sex-specific differences in overall and region-specific vertebral counts, male and female pipefish differ significantly in the relative lengths of their trunk and tail regions, consistent with region-specific selection pressures in the two sexes. Male pipefish show significant growth allometry, with disproportionate growth in the brooding tail region relative to the trunk, resulting in increasingly skewed region-specific sexual size dimorphism with increasing body size, a pattern consistent across five study populations. Sex-specific differences in patterns of growth in S. typhle support the hypothesis that fecundity selection can contribute to the evolution of sexual size dimorphism.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ahnesjö I (1992a) Fewer newborn result in superior juveniles in the paternally brooding pipefish Syngnathus typhle L. J Fish Biol 41:53–63

    Article  Google Scholar 

  • Ahnesjö I (1992b) Consequences of male brood care; weight and number of newborn in a sex—role reversed pipefish. Funct Ecol 6:274–281

    Article  Google Scholar 

  • Ahnesjö I (1995) Temperature affects male and female potential reproductive rates differently in the sex-role reversed pipefish. Behav Ecol 6:229–233

    Article  Google Scholar 

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

    Google Scholar 

  • Asano H (1977) On the tendencies of differentiation in the composition of the vertebral number of teleostean fishes. Mem Fac Agric Kinki Univ 10:29–37

    Google Scholar 

  • Berglund A (1991) Egg competition in a sex-role reversed pipefish: Subdominant females trade reproduction for growth. Evolution 45:770–774

    Article  Google Scholar 

  • Berglund A, Rosenqvist G (2001) Male pipefish prefer dominant over attractive females. Behav Ecol 12:402–406

    Article  Google Scholar 

  • Berglund A, Rosenqvist G (2003) Sex role reversal in pipefish. Adv Stud Behav 32:131–167

    Article  Google Scholar 

  • Berglund A, Rosenqvist G, Svensson I (1986) Mate choice, fecundity and sexual dimorphism in 2 pipefish species (Syngnathidae). Behav Ecol Sociobiol 19(4):301−307

    Google Scholar 

  • Bergmann PJ, Melin AD, Russell AP (2006) Differential segmental growth of the vertebral column of the rat (Rattus norvegicus). Zoology 109:54–65

    Article  PubMed  Google Scholar 

  • Bernet P, Rosenqvist G, Berglund A (1998) Female-female competition affects female ornamentation in the sex-role reversed pipefish Syngnathus typhle. Behaviour 135(5):535−550

    Google Scholar 

  • Blanckenhorn WU (2000) The evolution of body size: what keeps organisms small? Q Rev Biol 75:385–407

    Article  PubMed  CAS  Google Scholar 

  • Breder C, Rosen D (1966) Modes of reproduction in fishes. Natural History Press, New York

    Google Scholar 

  • Darwin C (1871) The descent of man, and selection in relation to sex. Murray, London

    Book  Google Scholar 

  • Dawson C (1986) Fishes of the north-eastern Atlantic and the Mediterranean. UNESCO, Paris

    Google Scholar 

  • Deane EE, Woo NYS (2009) Modulation of fish growth hormone levels by salinity, temperature, pollutants and aquaculture related stress: a review. Rev Fish Biol Fisher 19:97–120

    Article  Google Scholar 

  • Development Core Team R (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Duncker G (1908) Syngnathiden Studien. I. Variation und Modifikation bei Siphonostoma typhle L. Jahrb Hamburg Wissensc Anst 25:1–115

    Google Scholar 

  • Gould S (2002) The structure of evolutionary theory. Harvard, Cambridge

    Google Scholar 

  • Gould S, Lewontin R (1979) The spandrels of San Marco and the panglossian paradigm: a critique of the adaptationist programme. Proc R Soc Lond B Biol 205:581–598

    Article  CAS  Google Scholar 

  • Grande L, Bemis W (1998) A comprehensive phylogenetic study of amiid fishes (Amiidae) based on comparative skeletal anatomy. An empirical search for interconnected patterns of natural history. J Vertebr Paleontol 18:1–690

    Article  Google Scholar 

  • Hart J (1973) Pacific fishes of Canada. Fish Res Board Can Bull 180:740 pp

    Google Scholar 

  • Head JJ, Polly PD (2007) Dissociation of somatic growth from segmentation drives gigantism in snakes. Biol Lett 3:296–298

    Article  PubMed  Google Scholar 

  • Herald E (1941) A systematic analysis of variation in the western American pipefish, Syngnathus californiensis. Stanford Ichthyol Bull 2:49–73

    Google Scholar 

  • Hoffman E, Mobley K, Jones AG (2006) Male pregnancy and the evolution of body segmentation in seahorses and pipefishes. Evolution 60:404–411

    PubMed  Google Scholar 

  • Klingenberg CP (2005) Developmental constraints, modules, and evolvability. In: Hallgrimsson B, Hall BK (eds) Variation. A central concept in biology. Elsevier, Academic Press, Oxford, pp 219–248

    Google Scholar 

  • Lankford TE, Targett TE (1994) Sustainability of estuarine nursery zones for juvenile weakfish (Cynoscion regalis): effects of temperature and salinity on feeding, growth and survival. Mar Biol 119(4):611–620

    Article  Google Scholar 

  • Lindsey CC (1975) Pleomerism, the widespread tendency among related fish species for vertebral number to be correlated with maximum body length. J Fish Res Board Can 32:2453–2469

    Article  Google Scholar 

  • Madsen T, Shine R (1994) Costs of reproduction influence the evolution of sexual size dimorphism in snakes. Evolution 48:1389–1397

    Article  Google Scholar 

  • Mayr E (1972) Sexual selection and natural selection. In: Campbell B (ed) Sexual selection and the descent of man. Heinemann, London, pp 87–104

    Google Scholar 

  • Müller J, Scheyer T, Head JJ et al (2010) Homeotic effects, somitogenesis and the evolution of vertebral numbers in recent and fossil amniotes. PNAS 107(5):2118–2123

    Article  PubMed  Google Scholar 

  • Parra-Olea G, Wake DB (2001) Extreme morphological and ecological homoplasy in tropical salamanders. Proc Natl Acad Sci 98(14):7888–7891

    Article  PubMed  CAS  Google Scholar 

  • Polly DP, Head JJ, Cohn M (2001) Testing modularity and dissociation: the evolution of regional proportions in snakes. In: Zelditch M (ed) Beyond heterochrony: the evolution of development. Wiley-Liss, Inc, New York, pp 305–335

    Google Scholar 

  • Rispoli VF, Wilson AB (2008) Sexual size dimorphism predicts the frequency of multiple mating in the sex-role reversed pipefish Syngnathus typhle. J Evol Biol 21:30–38

    PubMed  CAS  Google Scholar 

  • Romer A (1970) The vertebrate body, 4th edn. Saunders, Philadelphia

    Google Scholar 

  • Shine R (2000) Vertebral numbers in male and female snakes: the roles of natural, sexual and fecundity selection. J Evol Biol 13:455–465

    Article  Google Scholar 

  • Springer VG (1971) Revision of the fish genus Ecsenius (Blenniidae, Bleniinae, Salariini). Smithson Contrib Zool 72:1–74

    Article  Google Scholar 

  • Vincent A, Berglund A, Ahnesjö I (1995) Reproductive ecology of five pipefish species in one eelgrass meadow. Environ Biol Fish 44:347–361

    Article  Google Scholar 

  • Wake D (1966) Comparative osteology and evolution of the lungless salamanders, family Plethodontidae. Mem S Calif Acad Sci 4:1–111

    Google Scholar 

  • Ward AB, Brainerd EL (2007) Evolution of axial patterning in elongate fishes. Biol J Linn Soc 90:97–116

    Article  Google Scholar 

  • Warton DI, Olmerod J (2005) Smatr v2.1. University of New South Wales, Sydney

    Google Scholar 

  • Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev 81:259–291

    Article  PubMed  Google Scholar 

  • Wilson AB, Eigenmann Veraguth I (2010) The impact of Pleistocene glaciation across the range of a widespread European coastal species. Mol Ecol 19:4535–4553

    Article  PubMed  CAS  Google Scholar 

  • Wilson AB, Vincent A, Ahnesjö I, Meyer A (2001) Male pregnancy in seahorses and pipefishes (family Syngnathidae): rapid diversification of paternal brood pouch morphology inferred from a molecular phylogeny. J Hered 92:159–166

    Article  PubMed  CAS  Google Scholar 

  • Wilson AB, Ahnesjö I, Vincent A, Meyer A (2003) The dynamics of male brooding, mating patterns and sex-roles in pipefishes and seahorses (Family Syngnathidae). Evolution 57:1374–1386

    PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank to Ingrid Ahnesjö, Murat Bilecenoglu, Iris Eigenmann, Nathalie Feiner, Jorge Gonçalves, Laurent Leveque, Federico Riccato, Valeria Rispoli, and Johan Wenngren for their help, efforts and time investments during field work. We are grateful to the Dipartimento di Scienze Ambientali (Università Ca’ Foscari), the Askö Laboratory, Klubban Biological Station, and the Roscoff Biological Station for the use of their facilities. Many thanks to Ingrid Ahnesjö, Christian Klingenberg, Marcelo Sánchez-Villagra, Lukas Rüber, and Lorenzo Tanadini for discussion and suggestions. Our special thanks go to Wolf Blanckenhorn for his statistical advice and to Jonathan Ready, INCOFISH project (EC project PL003739) for providing environmental data for sampling localities. The study was funded by the University of Zurich Forschungskredit, the Swiss Academy of Sciences and the Swiss National Science Foundation.

Author information

Author notes

  1. Kai N. Stölting

    Present address: Department of Biology, Unit of Ecology and Evolution, University of Fribourg, Chemin du Musée 10, 1700, Fribourg, Switzerland

Authors and Affiliations

  1. Institute of Evolutionary Biology and Environmental Studies, University of Zürich, Winterthurerstrasse 190, 8057, Zürich, Switzerland

    Jasmin D. Winkler, Kai N. Stölting & Anthony B. Wilson

Authors
  1. Jasmin D. Winkler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kai N. Stölting
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anthony B. Wilson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anthony B. Wilson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Winkler, J.D., Stölting, K.N. & Wilson, A.B. Sex-specific responses to fecundity selection in the broad-nosed pipefish. Evol Ecol 26, 701–714 (2012). https://doi.org/10.1007/s10682-011-9516-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-011-9516-4

Keywords

Search

Navigation