The evolutionary radiation of syngnathids has been accompanied by a diversification of structures involved in parental care, from a hypothetical ancestral presenting a simple brooding structure. The architectural simplicity of Nerophis male brooding structures led to the hypothesis that the relationship between father and developing embryos was feeble, unlike that observed in syngnathids with brood pouches. Here, we show that males loose considerable weight during pregnancy, especially so when egg weight is low. These results highlight the possibility of a compensatory mechanism and help justify why males in the wild tend to select large and colourful females, which are more fecund and able to produce larger eggs. Together with available information on the mating system, we also discuss some of the interplaying reasons behind the observed sex role reversal and high sexual dimorphism in the worm pipefish.
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Berglund A, Rosenqvist G, Svensson I (1986) Reversed sex-roles and parental energy investment in zygotes of 2 pipefish (Syngnathidae) species marine ecology progress series. 29:209–215. doi:10.3354/meps029209
Carcupino M (2002) Functional significance of the male brood pouch in the reproductive strategies of pipefishes and seahorses: a morphological and ultrastructural comparative study on three anatomically different pouches. J Fish Biol 61:1465–1480. doi:10.1006/jfbi.2002.2160
Cunha M, Berglund A, Alves T, Monteiro NM (2016) Reduced cannibalism during male pregnancy. Behaviour 153:91–106. doi:10.1163/1568539x-00003328
Dzyuba BB, Van Look KJ, Kholodnyy VS, Satake N, Cheung S, Holt WV (2008) Variable sperm size and motility activation in the pipefish, Syngnathus abaster; adaptations to paternal care or environmental plasticity? Reprod Fertil Dev 20:474–482
Hamilton H et al (2017) Molecular phylogeny and patterns of diversification in syngnathid fishes. Mol Phylogenet Evol 107:388–403. doi:10.1016/j.ympev.2016.10.003
Herald ES (1959) From pipefish to seahorse: a study of phylogenetic relationships. Proc Natl Acad Sci USA 29:465–473
Kvarnemo C, Mobley KB, Partridge C, Jones AG, Ahnesjo I (2011) Evidence of paternal nutrient provisioning to embryos in broad-nosed pipefish. J Fish Biol 78:1725–1737. doi:10.1111/j.1095-8649.2011.02989.x
Lahaye J (1971) L'Ovogenèse chez Nerophis lumbriciformis (Pennant, 1776). Le cycle sexuel Cahiers De Biologie Marine 12:239–254
McCoy EE, Jones AG, Avise JC (2001) The genetic mating system and tests for cuckoldry in a pipefish species in which males fertilize eggs and brood offspring externally. Mol Ecol 10:1793–1800
Monteiro NM, Lyons DO (2012) Stronger sexual selection in warmer waters: the case of a sex role reversed pipefish. PLoS ONE 7. doi:10.1371/journal.pone.0044251
Monteiro N, Vieira M, Almada V (2002) The courtship behaviour of the pipefish Nerophis lumbriciformis: reflections of an adaptation to intertidal life. Acta Ethologica 4:109–111. doi:10.1007/s102110100048
Monteiro N, Almada V, Santos A, Vieira M (2001) The breeding ecology of the pipefish and its relation to latitude and water temperature. J Mar Biol Assoc U K 81:1031–1033
Monteiro N, Almada V, Vieira M (2005a) Implications of different brood pouch structures in syngnathid reproduction. J Mar Biol Assoc U K 85:1235–1241
Monteiro N, Almada V, Vieira M (2005b) Temporal patterns of breeding and recruitment in Nerophis lumbriciformis (Pisces; Syngnathidae) related to seawater temperatures. J Fish Biol 67:1475–1480. doi:10.1111/j.1095-8649.2005.00818.x
Monteiro N, Vieira M, Almada V (2005c) Homing behaviour and individual identification of the pipefish Nerophis lumbriciformis (Pisces: Syngnathidae): a true intertidal resident? Estuar Coast Shelf Sci 63:93–99. doi:10.1016/j.ecss.2004.10.012
Monteiro NM, Berglund A, Vieira MN, Almada VC (2006) Reproductive migrations of the sex role reversed pipefish (Pisces; Syngnathidae). J Fish Biol 69:66–74. doi:10.1111/j.1095-8649.2006.01064.x
Monteiro N, Silva R, Cunha M, Antunes A, Jones A, Vieira M (2013a) Validating the use of coloration patterns for individual recognition in the worm pipefish using a novel set of microsatellite markers. Mol Ecol Resour
Monteiro N, Vieira M, Lyons D (2013b) Operational sex ratio, reproductive costs, and the potential for intrasexual competition. Biol J Linn Soc
Monteiro N, Carneiro D, Antunes A, Queiros N, Vieira N, Jones A (2017a) The lek mating system of the worm pipefish (Nerophis lumbriciformis): a molecular maternity analysis and test of the phenotype-linked fertility hypothesis. Mol Ecol 26:1371–1385. doi:10.1111/mec.13931
Monteiro N, Cunha M, Ferreira L, Vieira N, Antunes A, Lyons D, Jones AG (2017b) Parabolic variation in sexual selection intensity across the range of a cold-water pipefish: implications for susceptibility to climate change. Glob Chang Biol. doi:10.1111/gcb.13630
Paczolt KA, Jones AG (2010) Post-copulatory sexual selection and sexual conflict in the evolution of male pregnancy. Nature 464:401–404. doi:10.1038/nature08861
Partridge C, Shardo J, Boettcher A (2007) Osmoregulatory role of the brood pouch in the euryhaline gulf pipefish, Syngnathus scovelli. Comp Biochem Physiol Mol Integr Physiol 147:556–561
Ripley J (2009) Osmoregulatory role of the paternal brood pouch for two Syngnathus species. Comp Biochem Physiol
Roth O, Klein V, Beemelmanns A, Scharsack JP, TBH R (2012) Male pregnancy and biparental immune priming. Am Nat 180:802–814
Sagebakken G, Ahnesjo I, Braga Goncalves I, Kvarnemo C (2011) Multiply mated males show higher embryo survival in a paternally caring fish. Behav Ecol 22:625–629. doi:10.1093/beheco/arr023
Stolting K, Wilson A (2007) Male pregnancy in seahorses and pipefish: beyond the mammalian model BioEssays 29
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
Wilson A, 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
The Portuguese Foundation for Science and Technology funded Nuno Monteiro through a postdoc grant (SFRH/BPD/103829/2014). We thank the contribution of Clara Amorim, Anders Berglund and an anonymous reviewer, which helped improve the manuscript.
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Miranda, B., Vieira, N. & Monteiro, N. Pregnant pipefish with a simple brooding surface loose less weight when carrying heavier eggs: evidence of compensation for low oocyte quality?. acta ethol 20, 313–317 (2017). https://doi.org/10.1007/s10211-017-0268-1
- Differential allocation
- Sexual dimorphism
- Embryonic development
- Sexual selection