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

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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.

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References

  • 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 27:143–152

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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 24:888–897

    Article  Google Scholar 

  • Berglund A (1993) Risky sex: male pipefishes mate at random in the presence of a predator. Anim Behav 46:169–175

    Article  Google Scholar 

  • Berglund A (1994) The operational sex-ratio influences choosiness in a pipefish. Behav Ecol 5:254–258

    Article  Google Scholar 

  • Berglund A, Rosenqvist G (1993) Selective males and ardent females in pipefishes. Behav Ecol Sociobiol 32:331–336

    Article  Google Scholar 

  • Berglund A, Rosenqvist G (2001) Male pipefish prefer ornamented females. Anim Behav 61:345–350

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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 29:209–215

    Article  Google Scholar 

  • Berglund A, Rosenqvist G, Svensson I (1988) Multiple matings and paternal brood care in the pipefish Syngnathus typhle. Oikos 51:184–188

    Article  Google Scholar 

  • Berglund A, Rosenqvist G, Svensson I (1989) Reproductive success of females limited by males in two pipefish species. Am Nat 133:506–516

    Article  Google Scholar 

  • Berglund A, Rosenqvist G, Bernet P (1997) Ornamentation predicts reproductive success in female pipefish. Behav Ecol Sociobiol 40:145–150

    Article  Google Scholar 

  • Berglund A, Widemo MS, Rosenqvist G (2005) Sex-role reversal revisited: choosy females and ornamented, competitive males in a pipefish. Behav Ecol 16:649–655

    Article  Google Scholar 

  • 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 277:1581–1587

    Article  Google Scholar 

  • 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 22:165–173

    Article  Google Scholar 

  • Cotton S, Small J, Pomiankowski A (2006) Sexual selection and condition-dependent mate preferences. Curr Biol 16:R755–R765

    Article  CAS  PubMed  Google Scholar 

  • Cratsley CK, Lewis SM (2005) Seasonal variation in mate choice of Photinus ignitus fireflies. Ethology 111:89–100

    Article  Google Scholar 

  • Cunha M, Berglund A, Monteiro NM (2014) The intrinsically dynamic nature of mating patterns and sexual selection. Environ Biol Fish 98:1047–1058

    Article  Google Scholar 

  • 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 46:50–56

    Article  Google Scholar 

  • 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 86:347–352

    Article  Google Scholar 

  • 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 121:391–403

    Google Scholar 

  • 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 27:2457–2467

    Article  CAS  PubMed  Google Scholar 

  • Harrell, FE, Dupont C et al. (2014) Hmisc: Harrell miscellaneous, http://CRAN.R-project.org/package=Hmisc

  • 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 12:93–97

    Article  Google Scholar 

  • Henderson BA, Wong JL, Nepszy SJ (1996) Reproduction of walleye in Lake Erie: allocation of energy. Can J Fish Aquat Sci 53:127–133

    Article  Google Scholar 

  • 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 13:927–938

    Article  Google Scholar 

  • 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 46:357–365

    Article  Google Scholar 

  • 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 267:677–680

    Article  CAS  Google Scholar 

  • Jones AG, Rosenqvist G, Berglund A, Avise JC (2000b) Mate quality influences multiple maternity in the sex-role-reversed pipefish Syngnathus typhle. Oikos 90:321–326

    Article  Google Scholar 

  • 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 45:874–884

    Article  PubMed  Google Scholar 

  • Kasumovic MM, Bruce MJ, Andrade MCB, Herberstein ME (2008) Spatial and temporal demographic variation drives within-season fluctuations in sexual selection. Evolution 62:2316–2325

    Article  PubMed  Google Scholar 

  • 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 78:1725–1737

    Article  CAS  PubMed  Google Scholar 

  • 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 100:983–991

    Article  CAS  PubMed  Google Scholar 

  • McAllan BM, Geiser F (2006) Photoperiod and the timing of reproduction in Antechinus flavipes (Dasyuridae: Marsupialia). Mamm Biol 71:129–138

    Article  Google Scholar 

  • 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 68:52–60

    Article  Google Scholar 

  • 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 21:311–316

    Article  Google Scholar 

  • Mitrus C, Mitrus J, Sikora M (2012) Badge size and arrival time predict mating success of red-breasted flycatcher Ficedula parva males. Zool Sci 29:795–799

    Article  PubMed  Google Scholar 

  • 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 65:1169–1177

    Article  Google Scholar 

  • 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 4:67–78

    Article  PubMed  Google Scholar 

  • Møller AP (1994) Phenotype-dependent arrival time and its consequences in a migratory bird. Behav Ecol Sociobiol 35:115–122

    Article  Google Scholar 

  • 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 65:574–583

    Article  PubMed  Google Scholar 

  • Oring LW, Lank DB (1982) Sexual selection, arrival times, philopatry and site fidelity in the polyandrous spotted sandpiper. Behav Ecol Sociobiol 10:185–191

    Article  Google Scholar 

  • Parkos JJ, Wahl DH, Philipp DP (2011) Influence of behavior and mating success on brood-specific contribution to fish recruitment in ponds. Ecol Appl 21:2576–2586

    Article  PubMed  Google Scholar 

  • 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 63:345–354

    Article  Google Scholar 

  • 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 

  • Reichard M, Smith C, Bryja J (2008) Seasonal change in the opportunity for sexual selection. Mol Ecol 17:642–651

    Article  CAS  PubMed  Google Scholar 

  • Reynolds JD (1987) Mating system and nesting biology of the red-necked phalarope Phalaropus lobatus: what constrains polyandry? Ibis 129:225–242

    Article  Google Scholar 

  • Reznick D (1983) The structure of guppy life histories: the tradeoff between growth and reproduction. Ecology 64:862–873

    Article  Google Scholar 

  • Ripley JL, Foran CM (2006) Differential parental nutrient allocation in two congeneric pipefish species (Syngnathidae: Syngnathus spp.). J Exp Biol 209:1112–1121

    Article  PubMed  Google Scholar 

  • Robinson MR, van Doorn GS, Gustafsson L, Qvarnström A (2012) Environment-dependent selection on mate choice in a natural population of birds. Ecol Lett 15:611–618

    Article  PubMed  Google Scholar 

  • 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 129:744–752

    Article  Google Scholar 

  • Roff DA (2011) An allocation model of growth and reproduction in fish. Can J Fish Aquat Sci 40:1395–1404

    Article  Google Scholar 

  • 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 182:410–420

    Article  PubMed  Google Scholar 

  • 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 6:1160–1170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosenqvist G, Berglund A (2011) Sexual signals and mating patterns in Syngnathidae. J Fish Biol 78:1647–1661

    Article  CAS  PubMed  Google Scholar 

  • Rosenqvist G, Johansson K (1995) Male avoidance of parasitized females explained by direct benefits in a pipefish. Anim Behav 49:1039–1045

    Article  Google Scholar 

  • 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 48:405–413

    Article  Google Scholar 

  • 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 277:971–977

    Article  Google Scholar 

  • Sagebakken G, Ahnesjö I, Braga Goncalves I, Kvarnemo C (2011) Multiply mated males show higher embryo survival in a paternally caring fish. Behav Ecol 22:625–629

    Article  Google Scholar 

  • 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 81:1004–1012

    Article  PubMed  Google Scholar 

  • 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 267:2151–2155

    Article  CAS  Google Scholar 

  • Sefc KM, Hermann CM, Koblmüller S (2009) Mating system variability in a mouthbrooding cichlid fish from a tropical lake. Mol Ecol 18:3508–3517

    Article  CAS  PubMed  Google Scholar 

  • 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 74:1525–1533

    Article  Google Scholar 

  • Smith RJ, Moore FR (2003) Arrival fat and reproductive performance in a long-distance passerine migrant. Oecologia 134:325–331

    Article  PubMed  Google Scholar 

  • 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 78:1833–1846

    Article  CAS  PubMed  Google Scholar 

  • Sundin J, Sagebakken G, Kvarnemo C (2013) Female mate choice is not affected by mate condition in a fish with male care. Acta Ethol 16:189–194

    Article  Google Scholar 

  • Svensson I (1988) Reproductive costs in two sex-role reversed pipefish species (Syngnathidae). J Anim Ecol 32:929–942

    Article  Google Scholar 

  • Thorpe JE (1994) Reproductive strategies in Atlantic salmon, Salmo salar L. Aquac Res 25:77–87

    Article  Google Scholar 

  • Tobler M (2008) Divergence in trophic ecology characterizes colonization of extreme habitats. Biol J Linn Soc 95:517–528

    Article  Google Scholar 

  • Tomkins JL, Simmons LW (2002) Measuring relative investment: a case study of testes investment in species with alternative male reproductive tactics. Anim Behav 63:1009–1016

    Article  Google Scholar 

  • Vincent A, Ahnesjö I, Berglund A (1994) Operational sex ratios and behavioral sex differences in a pipefish population. Behav Ecol Sociobiol 34:435–442

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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 20:235–243

    Article  Google Scholar 

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Acknowledgements

Thanks to A. Berglund for contributing to project design and to S. van Leeuwen, C. Seger, and R. Höglund for the assistance with fish care and laboratory work. A. Berglund, K. Wedemeyer-Strombel, E. Rose, and A. Anderson and four anonymous reviewers commented on previous drafts of this manuscript. We thank Uppsala University-Campus Gotland for being able to use Ar research station.

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Correspondence to Sarah P. Flanagan.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All handling of fish was done under license Dnr 118-2008 from the Swedish Board of Agriculture. This work was partly supported by the Research Council of Norway through its Centres of Excellence funding scheme, project number 223257. SPF was supported by the National Science Foundation Graduate Research Fellowship under Grant No. DGE-1252521, supplemented by a GROW supplement in connection with the Norwegian Research Council. This work was conducted in part while SPF was a Postdoctoral Fellow at the National Institute for Mathematical and Biological Synthesis, an Institute sponsored by the National Science Foundation through NSF Award #DBI-1300426, with additional support from the University of Tennessee, Knoxville. This work was funded by grant number DEB-1119261 from the National Science Foundation to AGJ and by grant number DEB-1401688 to AGJ and SPF. The authors declare that they have no conflict of interest.

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Flanagan, S.P., Rosenqvist, G. & Jones, A.G. Mate quality and the temporal dynamics of breeding in a sex-role-reversed pipefish, S. typhle . Behav Ecol Sociobiol 71, 28 (2017). https://doi.org/10.1007/s00265-016-2255-3

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