Brooding fathers, not siblings, take up nutrients from embryos

Proceedings of the Royal Society B: Biological Sciences

Volumn 277, Issue 1683, 2010, Pages 971-977

  Sagebakken, Gry ^a   Ahnesjö, Ingrid ^b   Mobley, Kenyon B ^c   Gonçalves, Inês Braga ^a   Kvarnemo, Charlotta ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c UMEÅ UNIVERSITY   (Sweden)

Author keywords

Brood reduction; Embryo absorption; Female competition; Filial cannibalism; Nurse eggs; Post mating sexual selection

Indexed keywords

AMINO ACID; BROOD REARING; CANNIBALISM; EMBRYO; FEMALE BEHAVIOR; MUSCLE; NUTRIENT UPTAKE; OXYGEN; SEXUAL SELECTION; SIBLING; TELEOST;

ANIMALIA; SYNGNATHUS TYPHLE;

EID: 77949676410     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2009.1767     Document Type: Article

References (54)

1. Ahnesjö, I. 1992a Consequences of male brood care: weight and number of newborn in a sex-role reversed pipefish. Funct. Ecol. 6, 274-281. (doi:10.2307/2389517)
2. Ahnesjö, I. 1992b Fewer newborn result in superior juveniles in the paternally brooding pipefish Syngnathus typhle L. J. Fish. Biol. 41, 53-63. (doi:10.1111/j.1095-8649.1992. tb03868.x)
3. Ahnesjö, I. 1996 Apparent resource competition among embryos in the brood pouch of a male pipefish. Behav. Ecol. Sociobiol. 38, 167-172. (doi:10.1007/ s002650050229)
4. Azzarello, M. Y. 1991 Some questions concerning the Syngnathidae brood pouch. Bull Mar. Sci. 49, 741-747.
5. Berglund, A. & Rosenqvist, G. 1993 Selective males and ardent females in pipefishes. Behav. Ecol. Sociobiol. 32, 331-336. (doi:10.1007/BF00183788)
6. Berglund, A., Rosenqvist, G. & Svensson, I. 1986 Mate choice, fecundity and sexual dimorphism in two pipefish species (Syngnathidae). Behav. Ecol. Sociobiol. 19, 301-307. (doi:10.1007/BF00300646)
7. Berglund, A., Rosenqvist, G. & Svensson, I. 1989 Reproductive success of females limited by males in two pipefish species. Am. Nat. 133, 506-516. (doi: 10.1086/284932)
8. Bonabeau, E., Deneubourg, J. L. & Theraulaz, G. 1998 Within-brood competition and the optimal partitioning of parental investment. Am. Nat. 152, 419-427. (doi:10.1086/286179)
9. Brockelman, W. Y. 1975 Competition, the fitness of offspring, and optimal clutch size. Am. Nat. 109, 677-699. (doi:10.1086/283037)
10. Byrne, M. 1996 Viviparity and intragonadal cannibalism in the diminutive sea stars Patiriella vivipara and P. parvivipara (family Asterinidae). Mar. Biol. 125, 551-567.
11. Carcupino, M., Baldacci, A., Mazzini, M. & Franzoi, R 1997 Morphological organization of the male brood pouch epithelium of Syngnathus abaster Risso (Teleostea, Syngnathidae) before, during, and after egg incubation. Tissue Cell 29, 21-30. (doi:10.1016/S00408166(97)80068-7)
12. Carcupino, M., Baldacci, A., Mazzini, M. & Franzoi, R 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:10.1111/j.1095-8649.2002. tb02490.x)
13. Clutton-Brock, T. H. 1991 The evolution of parental care. Princeton, NJ: Princeton University Press.
14. Cubillos, V. M., Chaparro, O. R., Montiel, Y. A. & Veliz, D. 2007 Unusual source of food: impact of dead siblings on encapsulated embryo development of Crepipatella fecunda (Gastropoda: Calyptraeidae). Mar. Freshw. Res. 58, 1152-1161. (doi:10.1071/MF07094)
15. Dawson, C. E. 1985 Indo-pacific pipefishes (Red Sea to the Americas). Ocean Springs, MS: The Gulf Coast Research Laboratory.
16. Dzyuba, B., Van Look, K. J. W., Cliffe, A., Koldewey, H. J. & Holt, W. V. 2006 Effect of parental age and associated size on fecundity, growth and survival in the yellow seahorse Hippocampus kuda. J. Exp. Biol. 209, 3055-3061. (doi:10.1242/jeb.02336)
17. Forbes, L. S. & Lamey, T. C. 1996 Insurance, developmental accidents, and the risks of putting all your eggs in one basket. J. Theor. Biol. 180, 247-256. (doi:10.1006/jtbi. 1996.0100)
18. Forbes, L. S. & Mock, D. W. 1998 Parental optimism and progeny choice: when is screening for offspring quality affordable? J. Theor. Biol. 192, 3-14. (doi:10.1006/jtbi. 1997.0596)
19. Gilmore, R. G. 1993 Reproductive biology of lamnoid sharks. Environ. Biol. Fish. 38, 95-114. (doi:10.1007/ BF00842907)
20. Haig, D. 1990 Brood reduction and optimal parental investment when offspring differ in quality. Am. Nat. 136, 550-556. (doi:10.1086/285113)
21. Haig, D. 1992 Brood reduction in gymnosperms. In Cannibalism: ecology and evolution among diverse taxa (eds M. A. Elgar & B. J. Crespi), pp. 63-84. Oxford, UK: Oxford University Press.
22. 14C]alpha amino isobutyric acid. Comp. Biochem. Physiol. 69A, 603-603. (doi:10.1016/0300-9629(81)93030-9)
23. Jones, A. G., Rosenqvist, G., Berglund, A. & Avise, J. C. 1999a Clustered microsatellite mutations in the pipefish Syngnathus typhle. Genetics 152, 1057-1063.
24. Jones, A. G., Rosenqvist, G., Berglund, A. & Avise, J. C. 1999b The genetic mating system of a sex-role-reversed pipefish (Syngnathus typhle): a molecular inquiry. Behav. Ecol. Sociobiol. 46, 357-365. (doi: 10.1007/ s002650050630)
25. Klug, H. & Bonsall, M. B. 2007 When to care for, abandon, or eat your offspring: the evolution of parental care and filial cannibalism. Am. Nat. 170, 886-901. (doi: 10. 1086/522936)
26. Lamey, T. C., Evans, R. M. & Hunt, J. D. 1996 Insurance reproductive value and facultative brood reduction. Oikos 77, 285-290. (doi: 10.2307/3546067)
27. Lessells, C. M. 2002 Parentally biased favoritism: why should parents specialize in caring for different offspring? Phil. Trans. R. Soc. Lond. B 357, 381-403. (doi:10.1098/ rstb.2001.0928)
28. Lindström, K. 2000 The evolution of filial cannibalism and female mate choice strategies as resolutions to sexual conflict in fishes. Evolution 54, 617-627. (doi:10.1554/ 0014-3820(2000)054 [0617:TEOFCA]2.0.CO;2)
29. Lloyd, D. G. 1987 Selection of offspring size at independence and other size-versus-number strategies. Am. Nat. 129, 800-817. (doi:10.1086/284676)
30. Manica, A. 2002 Filial cannibalism in teleost fish. Biol. Rev. 77, 261-277. (doi:10.1017/S1464793101005905)
31. Mock, D. W. 2004 More than kin and less than kind. The evolution of family conflict. Cambridge, MA: The Belknap Press of Harvard University Press.
32. Mock, D. W. & Forbes, L. S. 1995 The evolution of parental optimism. Trends Ecol. Evol. 10, 130-134. (doi:10.1016/ S0169-5347(00)89014-X)
33. Mock, D. W. & Parker, G. A. 1998 Siblicide, family conflict and the evolutionary limits of selfishness. Anim. Behav. 56, 1-10. (doi:10.1006/anbe. l998.0842)
34. Nussbaum, R. A. & Schultz, D. L. 1989 Coevolution of parental care and egg size. Am. Nat. 133, 591-603. (doi:10.1086/284939)
35. Parker, G. A., Royle, N. J. & Hartley, I. R. 2002 Intrafamilial conflict and parental investment: a synthesis. Phil. Trans. R. Soc. Lond. B 357, 295-307. (doi:10.1098/rstb. 2001.0950)
36. Quast, W. D. & Howe, N. R. 1980 The osmotic role of the brood pouch in the pipefish Syngnathus scovelli. Comp. Biochem. Physiol. 67A, 675-678. doi:10.1016/03009629(80)90259-5)
37. Rice, W. R. 1989 Analyzing tables of statistical tests. Evolution 43, 223-225. (doi:10.2307/2409177)
38. Ripley, J. L. & Foran, C. M. 2006 Differential parental nutrient allocation in two congeneric pipefish species (Syngnathidae: Syngnathus spp.). J. Exp. Biol. 209, 1112-1121. (doi:10.1242/jeb.02119)
39. Ripley, J. L. & Foran, C. M. 2009 Direct evidence for embryonic uptake of paternally-derived nutrients in two pipefishes (Syngnathidae: Syngnathus spp.). J. Comp. Physiol. B 179, 325-333. (doi: 10.1007/s00360- 0080316-2)
40. Sachs, J. L., Mueller, U. G., Wilcox, T. P. & Bull, J. J. 2004 The evolution of cooperation. Q. Rev. Biol. 79, 136-160. (doi:0033-5770/2004/7902- 0001)
41. Sargent, R. C. 1992 Ecology of filial cannibalism in fishes: theoretical perspectives. In Cannibalism: ecology and evolution among diverse taxa (eds M. A. Elgar & B. J. Crespi), pp. 38-62. Oxford, UK: Oxford University Press.
42. Sasvari, L., Hegyi, Z. & Peczely, P. 1999 Brood reduction in white storks mediated through asymmetries in plasma testosterone concentrations in chicks. Ethology 105, 569-582. (doi:10.1046/j.1439-0310.1999. 00439.x)
43. Sinervo, B. & McEdward, L. R. 1988 Developmental consequences of an evolutionary change in egg size: an experimental test. Evolution 42, 885-899. (doi:10.2307/ 2408906)
44. Stanback, M. T. & Koenig, W. D. 1992 Cannibalism in birds. In Cannibalism: ecology and evolution among diverse taxa (eds M. A. Elgar & B. J. Crespi), pp. 277-298. Oxford, UK: Oxford University Press.
45. Stölting, K. K. & Wilson, A. B. 2007 Male pregnancy in seahorses and pipefish: beyond the mammalian model. Bioessays 29, 884-896. (doi:10.1002/bies.20626)
46. Trivers, R. L. 1972 Parental investment and sexual selection. In Sexual selection and the Descent of Man 1871-1971 (ed. B. Campbell), pp. 136-179. London, UK: Heinemann.
47. Trivers, R. L. 1974 Parent-offspring conflict. Am. Zool. 14, 249-264.
48. Vincent, A. C. J., Berglund, A. & Ahnesjö, I. 1995 Reproductive ecology of five pipefish species in one eelgrass meadow. Environ. Biol. Fish. 44, 347-361. (doi:10. 1007/BF00008250)
49. Watanabe, S., Kaneko, T. & Watanabe, Y. 1999 Immunocytochemical detection of mitochondria-rich cells in the brood pouch epithelium of the pipefish, Syngnathus schlegeli: structural comparison with mitochondria-rich cells in the gills and larval epidermis. Cell. Tissue Res. 295, 141-149. (doi:10.1007/s004410051220)
50. 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. J. Hered. 92, 159-166. (doi:10.1093/jhered/ 92.2.159)
51. Wilson, A. B., Ahnesjö, I., Vincent, A. C. J. & Meyer, A. 2003 The dynamics of male brooding, mating patterns, and sex roles in pipefishes and seahorses (family Syngnathidae). Evolution 57, 1374-1386.
52. Wourms, J. P. 1977 Reproduction and development in chondrichthyan fishes. Am. Zool. 17, 379-410.
53. Wourms, J. P. 1981 Viviparity: the maternal-fetal relationship in fishes. Am. Zool. 21, 473-515.
54. Young, E. C. & Millar, C. D. 2003 Siblicidal brood reduction in South Polar Skuas. NZ J. Zool. 30, 79-93.