Mate quality and the temporal dynamics of breeding in a sex-role-reversed pipefish, S. typhle

  • Sarah P. Flanagan
  • Gunilla Rosenqvist
  • Adam G. Jones
Original Article

Abstract

The spatiotemporal dynamics of receptivity and breeding date, coupled with individual-level quality and attractiveness, are centrally important to mating system dynamics. These topics have been investigated in some detail in birds, but much less work has been devoted to other taxonomic groups, and almost no work has addressed spatiotemporal factors and individual quality in sex-role-reversed taxa. The broad-nosed pipefish, Syngnathus typhle, provides an excellent opportunity to investigate these ideas in a sex-role-reversed fish. Here, we addressed three questions related to mating dynamics in S. typhle: (1) Do higher-quality males arrive earlier on the breeding grounds and mate first? (2) Are early-breeding males in better condition than later-breeding males? And (3) do mating events involving higher-quality males produce better clutches than mating events involving lower-quality males? We collected data from a field study and a laboratory breeding experiment to address our hypotheses. Our results show that larger males mate earlier than smaller males and that pregnant males have higher measures of condition compared to non-pregnant males. Moreover, our laboratory results demonstrate that pairings between larger males and preferred females yielded more offspring than pairings involving smaller males. In summary, the spatiotemporal dynamics of S. typhle breeding patterns, combined with variation in individual quality, play an important role in shaping mating systems and should be incorporated in future analyses of mating behavior and sexual selection in this interesting sex-role-reversed pipefish.

Significance statement

The breeding patterns of a species can fluctuate over time due to a number of factors, one of which is individual quality. Although the effects of both the timing of reproduction and female quality on mating systems have been studied in some species, they have been investigated primarily in isolation. Here, we demonstrate that individual quality and the timing of reproduction interact to affect reproductive success in a wild population of sex-role-reversed fish.

Keywords

Syngnathus typhle Reproductive success Condition Breeding date Mating systems 

References

  1. Aebischer A, Perrin N, Krieg M, Studer J, Meyer DR (1996) The role of territory choice, mate choice and arrival date on breeding success in the Savi’s warbler Locustella luscinioides. J Avian Biol 27:143–152CrossRefGoogle Scholar
  2. Ahnesjö I (1992a) Consequences of male brood care: weight and number of newborn in a sex-role reversed pipefish. Funct Ecol 6:274–281CrossRefGoogle Scholar
  3. Ahnesjö I (1992b) Fewer newborn result in superior juveniles in the paternally brooding pipefish Syngnathus typhle L. J Fish Biol 41:53–63CrossRefGoogle Scholar
  4. Aronsen T, Mobley KB, Berglund A, Sundin J, Billing AM, Rosenqvist G (2013) The operational sex ratio and density influence spatial relationships between breeding pipefish. Behav Ecol 24:888–897CrossRefGoogle Scholar
  5. Berglund A (1993) Risky sex: male pipefishes mate at random in the presence of a predator. Anim Behav 46:169–175CrossRefGoogle Scholar
  6. Berglund A (1994) The operational sex-ratio influences choosiness in a pipefish. Behav Ecol 5:254–258CrossRefGoogle Scholar
  7. Berglund A, Rosenqvist G (1993) Selective males and ardent females in pipefishes. Behav Ecol Sociobiol 32:331–336CrossRefGoogle Scholar
  8. Berglund A, Rosenqvist G (2001) Male pipefish prefer ornamented females. Anim Behav 61:345–350CrossRefGoogle Scholar
  9. Berglund A, Rosenqvist G, Svensson I (1986a) Mate choice, fecundity and sexual dimorphism in two pipefish species (Syngnathidae). Behav Ecol Sociobiol 19:301–307CrossRefGoogle Scholar
  10. Berglund A, Rosenqvist G, Svensson I (1986b) Reversed sex roles and parental energy investment in zygotes of two pipefish (Syngnathidae) species. Mar Ecol-Prog Ser 29:209–215CrossRefGoogle Scholar
  11. Berglund A, Rosenqvist G, Svensson I (1988) Multiple matings and paternal brood care in the pipefish Syngnathus typhle. Oikos 51:184–188CrossRefGoogle Scholar
  12. Berglund A, Rosenqvist G, Svensson I (1989) Reproductive success of females limited by males in two pipefish species. Am Nat 133:506–516CrossRefGoogle Scholar
  13. Berglund A, Rosenqvist G, Bernet P (1997) Ornamentation predicts reproductive success in female pipefish. Behav Ecol Sociobiol 40:145–150CrossRefGoogle Scholar
  14. Berglund A, Widemo MS, Rosenqvist G (2005) Sex-role reversal revisited: choosy females and ornamented, competitive males in a pipefish. Behav Ecol 16:649–655CrossRefGoogle Scholar
  15. Braga Goncalves I, Mobley KB, Ahnesjö I, Sagebakken G, Jones AG, Kvarnemo C (2010) Reproductive compensation in broad-nosed pipefish females. Proc R Soc Lond B 277:1581–1587CrossRefGoogle Scholar
  16. Colwell MA, Oring LW (1988) Sex ratios and intrasexual competition for mates in a sex-role reversed shorebird, Wilson’s phalarope (Phalaropus tricolor). Behav Ecol Sociobiol 22:165–173CrossRefGoogle Scholar
  17. Cotton S, Small J, Pomiankowski A (2006) Sexual selection and condition-dependent mate preferences. Curr Biol 16:R755–R765CrossRefPubMedGoogle Scholar
  18. Cratsley CK, Lewis SM (2005) Seasonal variation in mate choice of Photinus ignitus fireflies. Ethology 111:89–100CrossRefGoogle Scholar
  19. Cunha M, Berglund A, Monteiro NM (2014) The intrinsically dynamic nature of mating patterns and sexual selection. Environ Biol Fish 98:1047–1058CrossRefGoogle Scholar
  20. Dale J, Montgomerie R, Michaud D, Boag PT (1999) Frequency and timing of extrapair fertilisation in the polyandrous red phalarope (Phalaropus fulicarius). Behav Ecol Sociobiol 46:50–56CrossRefGoogle Scholar
  21. Dickerson BR, Brinck KW, Willson MF, Bentzen P, Quinn TP (2005) Relative importance of salmon body size and arrival time at breeding grounds to reproductive success. Ecology 86:347–352CrossRefGoogle Scholar
  22. Emlen ST, Wrege PH (2004) Size dimorphism, intrasexual competition, and sexual selection in wattled jacana (Jacana jacana), a sex-role-reversed shorebird in Panama. Auk 121:391–403Google Scholar
  23. Flanagan SP, Johnson JB, Rose E, Jones AG (2014) Sexual selection on female ornaments in the sex-role-reversed gulf pipefish (Syngnathus scovelli). J Evol Biol 27:2457–2467CrossRefPubMedGoogle Scholar
  24. Harrell, FE, Dupont C et al. (2014) Hmisc: Harrell miscellaneous, http://CRAN.R-project.org/package=Hmisc
  25. Hasselquist D, Wasson MF, Winkler DW (2001) Humoral immunocompetence correlates with date of egg-laying and reflects work load in female tree swallows. Behav Ecol 12:93–97CrossRefGoogle Scholar
  26. Henderson BA, Wong JL, Nepszy SJ (1996) Reproduction of walleye in Lake Erie: allocation of energy. Can J Fish Aquat Sci 53:127–133CrossRefGoogle Scholar
  27. Jann P, Blanckenhorn WU, Ward PI (2000) Temporal and microspatial variation in the intensities of natural and sexual selection in the yellow dung fly Scathophaga stercoraria. J Evol Biol 13:927–938CrossRefGoogle Scholar
  28. 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
  29. Jones AG, Rosenqvist G, Berglund A, Arnold SJ, Avise JC (2000a) The Bateman gradient and the cause of sexual selection in a sex-role-reversed pipefish. Proc R Soc Lond B 267:677–680CrossRefGoogle Scholar
  30. Jones AG, Rosenqvist G, Berglund A, Avise JC (2000b) Mate quality influences multiple maternity in the sex-role-reversed pipefish Syngnathus typhle. Oikos 90:321–326CrossRefGoogle Scholar
  31. Jones AG, Rosenqvist G, Berglund A, Avise JC (2005) The measurement of sexual selection using Bateman’s principles: an experimental test in the sex-role-reversed pipefish Syngnathus typhle. Integr Comp Biol 45:874–884CrossRefPubMedGoogle Scholar
  32. Kasumovic MM, Bruce MJ, Andrade MCB, Herberstein ME (2008) Spatial and temporal demographic variation drives within-season fluctuations in sexual selection. Evolution 62:2316–2325CrossRefPubMedGoogle Scholar
  33. Kvarnemo C, Mobley KB, Partridge C, Jones AG, Ahnesjö I (2011) Evidence of paternal nutrient provisioning to embryos in broad-nosed pipefish Syngnathus typhle. J Fish Biol 78:1725–1737CrossRefPubMedGoogle Scholar
  34. Laczi M, Hegyi G, Herényi M, Kiss D, Markó G, Nagy G, Rosivall B, Szöllősi E, Török J (2013) Integrated plumage colour variation in relation to body condition, reproductive investment and laying date in the collared flycatcher. Naturwissenschaften 100:983–991CrossRefPubMedGoogle Scholar
  35. McAllan BM, Geiser F (2006) Photoperiod and the timing of reproduction in Antechinus flavipes (Dasyuridae: Marsupialia). Mamm Biol 71:129–138CrossRefGoogle Scholar
  36. McPherson LR, Slotte A, Kvamme C, Meier S, Marshall CT (2011) Inconsistencies in measurement of fish condition: a comparison of four indices of fat reserves for Atlantic herring (Clupea harengus). ICES J Mar Sci 68:52–60CrossRefGoogle Scholar
  37. 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
  38. Mitrus C, Mitrus J, Sikora M (2012) Badge size and arrival time predict mating success of red-breasted flycatcher Ficedula parva males. Zool Sci 29:795–799CrossRefPubMedGoogle Scholar
  39. Mobley KB, Kvarnemo C, Ahnesjö I, Partridge C, Berglund A, Jones AG (2011) The effect of maternal body size on embryo survivorship in the broods of pregnant male pipefish. Behav Ecol Sociobiol 65:1169–1177CrossRefGoogle Scholar
  40. Mobley KB, Abou Chakra M, Jones AG (2014) No evidence for size-assortative mating in the wild despite mutual mate choice in sex-role-reversed pipefishes. Ecol Evol 4:67–78CrossRefPubMedGoogle Scholar
  41. Møller AP (1994) Phenotype-dependent arrival time and its consequences in a migratory bird. Behav Ecol Sociobiol 35:115–122CrossRefGoogle Scholar
  42. 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
  43. Oring LW, Lank DB (1982) Sexual selection, arrival times, philopatry and site fidelity in the polyandrous spotted sandpiper. Behav Ecol Sociobiol 10:185–191CrossRefGoogle Scholar
  44. Parkos JJ, Wahl DH, Philipp DP (2011) Influence of behavior and mating success on brood-specific contribution to fish recruitment in ponds. Ecol Appl 21:2576–2586CrossRefPubMedGoogle Scholar
  45. Partridge C, Ahnesjö I, Kvarnemo C, Mobley KB, Berglund A, Jones AG (2009) The effect of perceived female parasite load on post-copulatory male choice in a sex-role-reversed pipefish. Behav Ecol Sociobiol 63:345–354CrossRefGoogle Scholar
  46. R Core Team (2013) R: a language and environment for statistical computing. The R Foundation for Statistical Computing, Vienna http://www.R-project.org/Google Scholar
  47. Reichard M, Smith C, Bryja J (2008) Seasonal change in the opportunity for sexual selection. Mol Ecol 17:642–651CrossRefPubMedGoogle Scholar
  48. Reynolds JD (1987) Mating system and nesting biology of the red-necked phalarope Phalaropus lobatus: what constrains polyandry? Ibis 129:225–242CrossRefGoogle Scholar
  49. Reznick D (1983) The structure of guppy life histories: the tradeoff between growth and reproduction. Ecology 64:862–873CrossRefGoogle Scholar
  50. Ripley JL, Foran CM (2006) Differential parental nutrient allocation in two congeneric pipefish species (Syngnathidae: Syngnathus spp.). J Exp Biol 209:1112–1121CrossRefPubMedGoogle Scholar
  51. Robinson MR, van Doorn GS, Gustafsson L, Qvarnström A (2012) Environment-dependent selection on mate choice in a natural population of birds. Ecol Lett 15:611–618CrossRefPubMedGoogle Scholar
  52. Rockwell SM, Bocetti CI, Marra PP (2012) Carry-over effects of winter climate on spring arrival date and reproductive success in an endangered migratory bird, Kirtland’s warbler (Setophaga kirtlandii). Auk 129:744–752CrossRefGoogle Scholar
  53. Roff DA (2011) An allocation model of growth and reproduction in fish. Can J Fish Aquat Sci 40:1395–1404CrossRefGoogle Scholar
  54. Rose E, Paczolt KA, Jones AG (2013a) The contributions of premating and postmating selection episodes to total selection in sex-role-reversed gulf pipefish. Am Nat 182:410–420CrossRefPubMedGoogle Scholar
  55. Rose E, Paczolt KA, Jones AG (2013b) The effects of synthetic estrogen exposure on premating and postmating episodes of selection in sex-role-reversed gulf pipefish. Evol Appl 6:1160–1170CrossRefPubMedPubMedCentralGoogle Scholar
  56. Rosenqvist G, Berglund A (2011) Sexual signals and mating patterns in Syngnathidae. J Fish Biol 78:1647–1661CrossRefPubMedGoogle Scholar
  57. Rosenqvist G, Johansson K (1995) Male avoidance of parasitized females explained by direct benefits in a pipefish. Anim Behav 49:1039–1045CrossRefGoogle Scholar
  58. Rowe DK, Thorpe JE, Shanks AM (1991) Role of fat stores in the maturation of male Atlantic salmon (Salmo salar) parr. Can J Fish Aquat Sci 48:405–413CrossRefGoogle Scholar
  59. Sagebakken G, Ahnesjö I, Mobley KB, Braga Goncalves I, Kvarnemo C (2010) Brooding fathers, not siblings, take up nutrients from embryos. Proc R Soc Lond B 277:971–977CrossRefGoogle Scholar
  60. Sagebakken G, Ahnesjö I, Braga Goncalves I, Kvarnemo C (2011) Multiply mated males show higher embryo survival in a paternally caring fish. Behav Ecol 22:625–629CrossRefGoogle Scholar
  61. Saino N, Romano M, Ambrosini R, Rubolini D, Boncoraglio G, Caprioli M, Romano A (2012) Longevity and lifetime reproductive success of barn swallow offspring are predicted by their hatching date and phenotypic quality. J Anim Ecol 81:1004–1012CrossRefPubMedGoogle Scholar
  62. Sandvik M, Rosenqvist G, Berglund A (2000) Male and female mate choice affects offspring quality in a sex-role-reversed pipefish. Proc R Soc Lond B 267:2151–2155CrossRefGoogle Scholar
  63. Sefc KM, Hermann CM, Koblmüller S (2009) Mating system variability in a mouthbrooding cichlid fish from a tropical lake. Mol Ecol 18:3508–3517CrossRefPubMedGoogle Scholar
  64. 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
  65. Smith RJ, Moore FR (2003) Arrival fat and reproductive performance in a long-distance passerine migrant. Oecologia 134:325–331CrossRefPubMedGoogle Scholar
  66. Sogabe A, Ahnesjö I (2011) The ovarian structure and mode of egg production in two polygamous pipefishes: a link to mating pattern. J Fish Biol 78:1833–1846CrossRefPubMedGoogle Scholar
  67. Sundin J, Sagebakken G, Kvarnemo C (2013) Female mate choice is not affected by mate condition in a fish with male care. Acta Ethol 16:189–194CrossRefGoogle Scholar
  68. Svensson I (1988) Reproductive costs in two sex-role reversed pipefish species (Syngnathidae). J Anim Ecol 32:929–942CrossRefGoogle Scholar
  69. Thorpe JE (1994) Reproductive strategies in Atlantic salmon, Salmo salar L. Aquac Res 25:77–87CrossRefGoogle Scholar
  70. Tobler M (2008) Divergence in trophic ecology characterizes colonization of extreme habitats. Biol J Linn Soc 95:517–528CrossRefGoogle Scholar
  71. Tomkins JL, Simmons LW (2002) Measuring relative investment: a case study of testes investment in species with alternative male reproductive tactics. Anim Behav 63:1009–1016CrossRefGoogle Scholar
  72. Vincent A, Ahnesjö I, Berglund A (1994) Operational sex ratios and behavioral sex differences in a pipefish population. Behav Ecol Sociobiol 34:435–442CrossRefGoogle Scholar
  73. Vincent ACJ, Berglund A, Ahnesjö I (1995) Reproductive ecology of five pipefish species in one eelgrass meadow. Environ Biol Fish 44:347–361CrossRefGoogle Scholar
  74. Wendeln H (1997) Body mass of female common terns (Sterna hirundo) during courtship: relationships to male quality, egg mass, diet, laying date and age. Colon. Waterbird 20:235–243CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Sarah P. Flanagan
    • 1
    • 2
  • Gunilla Rosenqvist
    • 3
    • 4
  • Adam G. Jones
    • 1
  1. 1.Biology DepartmentTexas A&M UniversityCollege StationUSA
  2. 2.National Institute for Mathematical and Biological SynthesisUniversity of TennesseeKnoxvilleUSA
  3. 3.Centre for Biodiversity Dynamics Department of BiologyNorwegian University of Science and TechnologyTrondheimNorway
  4. 4.EBC, Uppsala UniversityVisbySweden

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