Evidence of paternal nutrient provisioning to embryos in broad-nosed pipefish Syngnathus typhle

Journal of Fish Biology

Volumn 78, Issue 6, 2011, Pages 1725-1737

  Kvarnemo, C ^a,b   Mobley, K B ^c,e   Partridge, C ^c,f   Jones, A G ^c   Ahnesjo I ^d  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c TEXAS A AND M UNIVERSITY   (United States)

^d UPPSALA UNIVERSITY   (Sweden)

^e UMEÅ UNIVERSITY   (Sweden)

^f WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Feeding of offspring; Paternal care; Radiolabelled amino acids and glucose; Syngnathidae; Viviparity

Indexed keywords

AMINO ACID; CARBON; DIAGNOSTIC AGENT; GLUCOSE; TRITIUM;

ANIMAL; ANIMAL EMBRYO; ARTICLE; BODY SIZE; EMBRYO DEVELOPMENT; MALE; METABOLISM; PHYSIOLOGY; REPRODUCTION; SMEGMAMORPHA;

AMINO ACIDS; ANIMALS; BODY SIZE; CARBON RADIOISOTOPES; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; GLUCOSE; MALE; REPRODUCTION; SMEGMAMORPHA; TRITIUM;

SYNGNATHIDAE; SYNGNATHUS TYPHLE;

EID: 79958261258     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/j.1095-8649.2011.02989.x     Document Type: Article

References (39)

1. Ahnesjö, I. (1992a). Fewer newborn result in superior juveniles in the paternally brooding pipefish Syngnathus typhle. Journal of Fish Biology 41 (Suppl. B), 53-63.
2. Ahnesjö, I. (1992b). Consequences of male brood care; weight and number of newborn in a sex-role reversed pipefish. Functional Ecology 6, 274-281.
3. Ahnesjö, I. (1995). Temperature affects male and female potential reproductive rates differently in the sex-role reversed pipefish Syngnathus typhle. Behavioral Ecology 6, 229-233.
4. Ahnesjö, I. (1996). Apparent resource competition among embryos in the brood pouch of a male pipefish. Behavioral Ecology and Sociobiology 38, 167-172.
5. Avise, J. C. & Liu, J.-X. (2010). Multiple mating and its relationship to alternative modes of gestation in male-pregnant versus female-pregnant fish species. Proceedings of the National Academy of Sciences 107, 18915-18920. DOI: 10.1073/pnas.1013786107.
6. Berglund, A., Rosenqvist, G. & Svensson, I. (1986). Reversed sex roles and parental energy investment in zygotes of two pipefish (Syngnathidae) species. Marine Ecology Progress Series 29, 209-215.
7. Berglund, A., Rosenqvist, G. & Svensson, I. (1988). Multiple matings and paternal brood care in the pipefish, Syngnathus typhle. Oikos 51, 184-188.
8. Braga Goncalves, I. (2010). Egg size evolution and paternal care in pipefishes. PhD Thesis, Gothenburg, University of Gothenburg, Sweden.
9. Braga Goncalves, I., Mobley, K. B., Ahnesjö, I., Sagebakken, G., Jones, A. G. & Kvarnemo, C. (2010). Reproductive compensation in broad-nosed pipefish females. Proceedings of the Royal Society B 277, 1581-1587. DOI: 10.1098/rspb.2009.2290.
10. Carcupino, M., Baldacci, A., Mazzini, M. & Franzoi, P. (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. Journal of Fish Biology 61, 1465-1480.
11. Crespi, B. & Semeniuk, C. (2004). Parent-offspring conflict in the evolution of vertebrate reproductive mode. American Naturalist 163, 635-653.
12. Dawson, C. E. (1985). Indo-Pacific Pipefishes, Red Sea to the Americas. Ocean Springs, MS: The Gulf Coast Research Laboratory.
13. Foster, S. J. & Vincent, A. C. J. (2004). Life history and ecology of seahorses, implications for conservation and management. Journal of Fish Biology 65, 1-61. DOI: 10.1111/j. 1095-8649.2004.00429.x.
14. 14C)-alpha-amino-isobutyric acid. Comparative Biochemistry and Physiology A 69, 603-604.
15. Herald, E. S. (1959). From pipefish to seahorse - a study of phylogenetic relationships. Proceedings of the Californian Academy of Sciences 29, 465-473.
16. Jones, A. G., Rosenqvist, G., Berglund, A. & Avise, J. C. (1999). The genetic mating system of a sex-role reversed pipefish (Syngnathus typhle): a molecular inquiry. Behavioral Ecology and Sociobiology 46, 357-365.
17. Kamler, E. (2005). Parent-egg-progeny relationships in teleost fishes: an energetic perspective. Reviews in Fish Biology and Fisheries 15, 399-421. DOI: 10.1007/s11160-006-0002-y.
18. Kamler, E. (2008). Resource allocation in yolk-feeding fish. Reviews in Fish Biology and Fisheries 18, 143-200. DOI: 10.1007/s11160-007-9070-x.
19. Kolm, N. & Ahnesjö, I. (2005). Do egg size and parental care coevolve in fishes? Journal of Fish Biology 66, 1499-1515. DOI: 10.1111/j.1095-8649.2005.00777.x.
20. Korsgaard, B. (1991). Metabolism of larval turbot Scophthalmus maximus (L.) and uptake of amino acids from seawater studied by autoradiographic and radiochemical methods. Journal of Experimental Marine Biology and Ecology 148, 1-10.
21. Laksanawimol, P., Damrongphol, P. & Kruatrachue, M. (2006). Alteration of the brood pouch morphology during gestation of male seahorses, Hippocampus kuda. Marine and Freshwater Research 57, 497-502.
22. Linton, J. R. & Soloff, B. L. (1964). The physiology of the brood pouch of the male sea horse Hippocampus erectus. Bulletin of Marine Science of the Gulf and Caribbean 14, 45-61.
23. Mank, J. E. & Avise, J. C. (2006). Supertree analyses of the roles of viviparity and habitat in the evolution of atherinomorph fishes. Journal of Evolutionary Biology 19, 734-740.
24. Marsh-Matthews, E., Brooks, M., Deaton, R. & Tan, H. (2005). Effects of maternal and embryo characteristics on post-fertilization provisioning in fishes of the genus Gambusia. Oecologia 144, 12-24.
25. Mobley, K. B., Kvarnemo, C., Ahnesjö, I., Partridge, C., Berglund, A. & Jones, A. G. (2011). The effect of maternal body size on embryo survivorship in the broods of pregnant male pipefish. Behavioral Ecology and Sociobiology. (In press) DOI: 10.1007/s00265-010-1129-3.
26. Paczolt, K. A. & Jones, A. G. (2010). Post-copulatory sexual selection and sexual conflict in the evolution of male pregnancy. Nature 464, 401-404. DOI: 10.1038/nature08861.
27. Partridge, C. (2003). The reproductive physiology and histology of the gulf pipefish, Syngnathus scovelli. MSc Thesis, University of South Alabama, Mobile, SA, USA.
28. Partridge, C., Ahnesjö, I., Kvarnemo, C., Mobley, K. B., Berglund, A. & Jones, A. G. (2009). The effect of perceived female parasite load on post-copulatory male choice in a sex-role-reversed pipefish. Behavioral Ecology and Sociobiology 63, 345-354. DOI: 10.1007/s00265-008-0668-3.
29. Reznick, D. N., Mateos, M. & Springer, M. S. (2002). Independent origins and rapid evolution of the placenta in the fish genus Poeciliopsis. Science 298, 1018-1020.
30. Ripley, J. L. & Foran, C. M. (2006). Differential parental nutrient allocation in two congeneric pipefish species (Syngnathidae: Syngnathus spp.). Journal of Experimental Biology 209, 1112-1121. DOI: 10.1242/jeb.02119.
31. Ripley, J. L. & Foran, C. M. (2009). Direct evidence for embryonic uptake of paternally derived nutrients in two pipefishes (Syngnathidae: Syngnathus spp.). Journal of Comparative Physiology B 179, 325-333. DOI: 10.1007/s00360-008-0316-2.
32. Ripley, J. L., Williams, P. S. & Foran, C. M. (2010). Morphological and quantitative changes in paternal brood pouch vasculature during embryonic development in two Syngnathus pipefishes. Journal of Fish Biology 77, 67-79. DOI: 10.1111/j.1095-8649.2010.02659.x.
33. Rombough, P. J. (1988). Respiratory gas exchange, aerobic metabolism, and effects of hypoxia during early life. In Fish Physiology, Vol. 11, Part A (Hoar, W. S. & Randall, D. J., eds), pp. 59-161. London: Academic Press.
34. Rombough, P. J. (2007). Oxygen as a constraining factor in egg size evolution in salmonids. Canadian Journal of Fisheries and Aquatic Sciences 64, 692-699.
35. Rønnestad, I. & Fyhn, H. J. (1993). Metabolic aspects of free amino acids in developing marine fish eggs and larvae. Reviews in Fisheries Science 1, 239-259.
36. Sagebakken, G., Ahnesjö, I., Mobley, K. B., Braga Gonçalves, I. & Kvarnemo, C. (2010). Brooding fathers, not siblings, take up nutrients from embryos. Proceedings of the Royal Society B 277, 971-977. DOI: 10.1098/rspb.2009.1767.
37. Stölting, K. N. & Wilson, A. B. (2007). Male pregnancy in seahorses and pipefish: beyond the mammalian model. BioEssays 29, 884-896. DOI: 10.1002/bies.20626.
38. Vincent, A., Ahnesjö, I., Berglund, A. & Rosenqvist, G. (1992). Pipefishes and seahorses: are they all sex role reversed? Trends in Ecology & Evolution 7, 237-241. DOI: 10.1016/0169-5347 (92)90052-D.
39. Wilson, A. B., 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. Journal of Heredity 92, 159-166.