Environmental Biology of Fishes

, Volume 98, Issue 4, pp 1047–1058 | Cite as

The intrinsically dynamic nature of mating patterns and sexual selection

  • M. Cunha
  • A. Berglund
  • N. M. Monteiro


Selection processes are influenced by both biotic and abiotic variables, most of which seasonally fluctuate. Therefore, selection may also vary temporally. Specifically, sexual selection, an integral component of natural selection, will inevitably exhibit temporal variation but the scale at which these changes occur are still not well understood. In this study, performed on a wild population of the sex-role reversed black striped pipefish Syngnathus abaster (Risso, 1827), we contrast variables such as male reproductive success, mating success, female investment, mate choice and operational sex ratio between two periods, either near the onset or end of the breeding season. Sexual selection is stronger early in the breeding season. Male reproductive and mating success are significantly affected by male size during the onset of the breeding season but not during the end. Moreover, we found that larger females reproduce mainly during the onset while smaller females had increased chances of reproducing towards the end. As our sampling was performed in two consecutive years, it could be argued that our results stem primarily from between-year variation. Nevertheless, variation in demographic parameters from the onset to the end of the breeding season is similar to that observed in past sampling events. Hence, we suggest that the change in mating patterns within the breeding season derives from seasonal fluctuations in several abiotic (e.g., temperature) and biotic variables (e.g., operational sex ratio), rendering the expression of selective forces, such as sexual selection, inherently dynamic.


Mating system Female investment Mate choice Reproduction Variation Selection 



We thank the contributions of the editor and two anonymous referees, for their valuable comments on the manuscript. This study was partially funded by the Portuguese Foundation for Science and Technology (FCT) through the R&D project PTDC/AAC-CLI/112936/2009 and the Project “Genomics Applied To Genetic Resources” co-financed by North Portugal Regional Operational Programme 2007/2013 (ON.2 – O Novo Norte), under the National Strategic Reference Framework (NSRF), through the European Regional Development Fund (ERDF). The Portuguese Foundation for Science and Technology funded Nuno Monteiro through “Programa Ciência (2009)” and Mário Cunha through the PhD grant SFRH/BD/87616/2012.

Supplementary material

10641_2014_338_MOESM1_ESM.doc (52 kb)
ESM 1 (DOC 51 kb)


  1. Andersson M, Simmons LW (2006) Sexual selection and mate choice. Trends Ecol Evol 21:296–302CrossRefPubMedGoogle Scholar
  2. Begovac PC, Wallace RA (1988) Stages of oocyte development in the pipefish, syngnathus scovelli. J Morphol 197:353–369CrossRefGoogle Scholar
  3. Berglund A, Rosenqvist G (1990) Male limitation of female reproductive success in a pipefish: effects of body-size differences. Behav Ecol Sociobiol 27:129–133CrossRefGoogle Scholar
  4. Berglund A, Rosenqvist G, Svensson I (1986) Mate choice, fecundity and sexual dimorphism in two pipefish species (Syngnathidae). Behav Ecol Sociobiol 19:301–307CrossRefGoogle Scholar
  5. Berglund A, Rosenqvist G, Robinson-Wolrath S (2006) Food or sex—males and females in a sex role reversed pipefish have different interests. Behav Ecol Sociobiol 60:281–287CrossRefGoogle Scholar
  6. Braga Goncalves I, Ahnesjö I, Kvarnemo C (2011) The relationship between female body size and egg size in pipefishes. J Fish Biol 78:1847–1854CrossRefPubMedGoogle Scholar
  7. Chaine AS, Lyon BE (2008) Adaptive plasticity in female mate choice dampens sexual selection on male ornaments in the lark bunting. Science 319:459–462CrossRefPubMedGoogle Scholar
  8. Cogliati KM, Neff BD, Balshine S (2013) High degree of paternity loss in a species with alternative reproductive tactics. Behav Ecol and Sociobiol 67(3):399–408CrossRefGoogle Scholar
  9. Cratsley CK, Lewis SM (2005) Seasonal variation in mate choice of photinus ignitus fireflies. Ethology 111:89–100CrossRefGoogle Scholar
  10. Diekmann OE, Gouveia L, Serrão EA, Van De Vilet MS (2009) Highly polymorphic microsatellite markers for the black striped pipefish, syngnathus abaster. Mol Ecol Resources 9:1460–1466CrossRefGoogle Scholar
  11. Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223CrossRefPubMedGoogle Scholar
  12. Estabrook G, Almada V, Almada F, Robalo J (2002) Analysis of conditional contingency using ACTUS2 with examples from studies of animal behavior. Acta Ethol 4:73–80CrossRefGoogle Scholar
  13. Forsgren E, Amundsen T, Borg AA, Bjelvenmark J (2004) Unusually dynamic sex roles in a fish. Nature 429:551–554CrossRefPubMedGoogle Scholar
  14. Jones AG (2005) GERUD2.0: a computer program for the reconstruction of parental genotypes from half-sib progeny arrays with known or unknown parents. Mol Ecol Notes 5:708–711CrossRefGoogle Scholar
  15. Jones AG, Avise JC (1997) Polygynandry in the dusky pipefish syngnathus floridae revealed by microsatellite DNA markers. Evolution 51:1611–1622CrossRefGoogle Scholar
  16. 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 92:150–158CrossRefPubMedGoogle Scholar
  17. Jones AG, Rosenqvist G, Berglund A, Avise JC (1999) The genetic mating system of a sex-role-reversed pipefish (Syngnathus typhle): a molecular inquiry. Behav Ecol Sociobiol 46:357–365CrossRefGoogle Scholar
  18. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program cervus accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106CrossRefPubMedGoogle Scholar
  19. Mattle B, Wilson AB (2009) Body size preferences in the pot-bellied seahorse hippocampus abdominalis: choosy males and indiscriminate females. Behav Ecol Sociobiol 63:1403–1410CrossRefPubMedCentralPubMedGoogle Scholar
  20. McAllan BM, Geiser F (2006) Photoperiod and the timing of reproduction in antechinus flavipes (Dasyuridae: Marsupialia). Mamm Biol 71:129–138Google Scholar
  21. Meirmans PG, Van Tienderen PH (2004) Genotype and genodive: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794CrossRefGoogle Scholar
  22. Milner RNC, Detto T, Jennions MD, Backwell PRY (2010) Experimental evidence for a seasonal shift in the strength of a female mating preference. Behav Ecol 21:311–316CrossRefGoogle Scholar
  23. Mobley KB, Jones AG (2007) Geographical variation in the mating system of the dusky pipefish (Syngnathus floridae). Mol Ecol 16:2596–2606CrossRefPubMedGoogle Scholar
  24. Mobley KB, Jones AG (2009) Environmental, demographic, and genetic mating system variation among five geographically distinct dusky pipefish (Syngnathus floridae) populations. Mol Ecol 18:1476–1490CrossRefPubMedGoogle Scholar
  25. Mobley KB, Kvarnemo C, Ahnesjö I, Partridge C, Berglund A, Jones AG (2011a) The effect of maternal body size on embryo survivorship in the broods of pregnant male pipefish. Behav Ecol Sociobiol 65:1169–1177CrossRefGoogle Scholar
  26. Mobley KB, Small CM, Jones AG (2011b) The genetics and genomics of Syngnathidae: pipefishes, seahorses and seadragons. J Fish Biol 78:1624–1646CrossRefPubMedGoogle Scholar
  27. Monteiro NM, Lyons DO (2012) Stronger sexual selection in warmer waters: the case of a Sex role reversed pipefish. PLoS ONE 7Google Scholar
  28. Monteiro NM, Almada V, Vieira M (2005) Implications of different brood pouch structures in syngnathid reproduction. J Mar Biol Ass UK 85:1235–1241CrossRefGoogle Scholar
  29. Monteiro NM, Vieira MN, Lyons DO (2013) Operational sex ratio, reproductive costs and the potential for intrasexual competition. Biol J Linn Soc 110:477–484CrossRefGoogle Scholar
  30. Naef-Daenzer B, Widmer F, Nuber M (2001) Differential post-fledging survival of great and coal tits in relation to their condition and fledging date. J Anim Ecol 70:730–738CrossRefGoogle Scholar
  31. Neff BD, Clare EL (2008) Temporal variation in cuckoldry and paternity in two sunfish species (Lepomis spp.) with alternative reproductive tactics. Can J of Zool 86:92–98CrossRefGoogle Scholar
  32. Olsson M, Wapstra E, Schwartz T, Madsen T, Ujvari B, Uller T (2011) In hot pursuit: fluctuating mating system and sexual selection in sand lizards. Evolution 65:574–583CrossRefPubMedGoogle Scholar
  33. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539CrossRefPubMedCentralPubMedGoogle Scholar
  34. Post E, Levin SA, Iwasa Y, Stenseth NC (2001) Reproductive asynchrony increases with environmental disturbance. Evolution 55:830–834CrossRefPubMedGoogle Scholar
  35. Reichard M, Smith C, Bryja J (2008) Seasonal change in the opportunity for sexual selection. Mol Ecol 17:642–651CrossRefPubMedGoogle Scholar
  36. Rispoli VF, Wilson AB (2007) Sexual size dimorphism predicts the frequency of multiple mating in the sex-role reversed pipefish Syngnathus typhle. J Evolution Biol 21:30–38Google Scholar
  37. Robinson MR, Sander van Doorn G, Gustafsson L, Qvarnström A (2012) Environment-dependent selection on mate choice in a natural population of birds. Ecol Lett 15:611–618CrossRefPubMedGoogle Scholar
  38. Rosenqvist G (1990) Male mate choice and female-female competition for mates in the pipefish Nerophis ophidion. Anim Behav 39:1110–1115CrossRefGoogle Scholar
  39. Saraiva JL, Barata EN, Canário AVM, Oliveira RF (2009) The effect of nest aggregation on the reproductive behaviour of the peacock blenny Salaria pavo. J Fish Biol 74:754–762CrossRefPubMedGoogle Scholar
  40. Saraiva JL, Pignolo G, Gonçalves D, Oliveira RF (2012) Interpopulational variation of the mating system in the peacock blenny Salaria pavo. Acta Ethol 15:25–31CrossRefGoogle Scholar
  41. Sárria MP, Santos MM, Reis-Henriques MA, Vieira NM, Monteiro NM (2011) Drifting towards the surface: A shift in newborn pipefish’s vertical distribution when exposed to the synthetic steroid ethinylestradiol Chemosphere 84:618–624 doi: 10.1016/j.chemosphere.2011.03.049
  42. Sekino M, Kakehi S (2012) PARFEX v1.0: an EXCEL™-based software package for parentage allocation. Conser Genet Resour 4:275–278CrossRefGoogle Scholar
  43. Siepielski AM, Dibattista JD, Carlson SM (2009) It’s about time: The temporal dynamics of phenotypic selection in the wild. Ecol Lett 12:1261–1276CrossRefPubMedGoogle Scholar
  44. Silva K, Monteiro N, Almada V, Vieira M (2006a) Early life history of Syngnathus abaster. J Fish Biol 68:80–86. doi: 10.1111/j.1095-8649.2005.00878.x CrossRefGoogle Scholar
  45. Silva K, Monteiro NM, Vieira MN, Almada VC (2006b) Reproductive behaviour of the black-striped pipefish Syngnathus abaster (Pisces; Syngnathidae). J Fish Biol 69:1860–1869CrossRefGoogle Scholar
  46. Silva K, Vieira MN, Almada VC, Monteiro NM (2007) The effect of temperature on mate preferences and female–female interactions in Syngnathus abaster. Anim Behav 74:1525–1533CrossRefGoogle Scholar
  47. Silva K, Vieira MN, Almada VC, Monteiro NM (2008) Can the limited marsupium space be a limiting factor for Syngnathus abaster females? Insights from a population with size-assortative mating. J Anim Ecol 77:390–394CrossRefPubMedGoogle Scholar
  48. Silva K, Almada VC, Vieira MN, Monteiro NM (2009) Female reproductive tactics in a sex-role reversed pipefish: scanning for male quality and number. Behav Ecol 20:768–772CrossRefGoogle Scholar
  49. Silva K, Vieira MN, Almada VC, Monteiro NM (2010) Reversing sex role reversal: compete only when you must. Anim Behav 79:885–893CrossRefGoogle Scholar
  50. Streatfeild CA, Mabry KE, Keane B, Crist TO, Solomon NG (2011) Intraspecific variability in the social and genetic mating systems of prairie voles, Microtus ochrogaster. Anim Behav 82:1387–1398CrossRefGoogle Scholar
  51. Watanabe S, Watanabe Y (2002) Relationship between male size and newborn size in the seaweed pipefish, Syngnathus schlegeli. Environ Biol Fish 65:319–325CrossRefGoogle Scholar
  52. Wilson AB (2009) Fecundity selection predicts Bergmann’s rule in syngnathid fishes. Mol Ecol 18:1263–1272CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  1. 1.CIBIO/InBIO, Centro de Investigação em Biodiversidade e Recursos GenéticosVairãoPortugal
  2. 2.Faculdade de Ciências da Universidade do PortoPortoPortugal
  3. 3.Department of Animal Ecology, Evolutionary Biology Centre (EBC)Uppsala UniversityUppsalaSweden
  4. 4.CEBIMED Faculdade de Ciências da SaúdeUniversidade Fernando PessoaPortoPortugal

Personalised recommendations