Embryonic developmental plasticity in the long-snouted seahorse (Hippocampus reidi, Ginsburg 1933) in relation to parental preconception diet
Francisco Otero-Ferrer A , Marisol Izquierdo A , Alireza Fazeli B and William V. Holt B CA Grupo de Investigación en Acuicultura (ULPGC), Parque Cientifico Tecnológico, Taliarte 35200, Telde (Las Palmas), España.
B Academic Unit of Reproductive and Developmental Medicine, University of Sheffield, Level 4, Jessop Wing, Tree Root Walk, Sheffield S10 2SF, UK.
C Corresponding author. Email: bill.holt@sheffield.ac.uk
Reproduction, Fertility and Development 28(7) 1020-1028 https://doi.org/10.1071/RD14169
Submitted: 22 May 2014 Accepted: 17 November 2014 Published: 17 December 2014
Abstract
The aim of the present study was to investigate the hypothesis that parental periconception nutrition in adult seahorses affects the development and growth of their offspring. We tested the hypothesis that because seahorse embryos develop inside the male’s brood pouch, manipulation of the male’s diet would affect offspring growth and development independently of the female’s diet. Adult males and females were fed separately with either wild-caught crustaceans or commercial aquarium diet for 1 month before conception to influence the periconception environment. Approximately 10 000 offspring were obtained from four different treatment groups (Male/Wild or Male/Commercial × Female/Wild or Female/Commercial). Weights, physical dimensions and fatty acid profiles of the newborns were determined. Offspring produced when the males receiving commercial diet were mated with wild-fed females were larger (P < 0.05) than those produced by wild-fed males. When both males and females were fed with commercial diet, their offspring were significantly smaller than those from the other treatment groups. When commercial diet-fed females were mated with wild-fed males, the offspring showed distortion of the snout : head length ratio. These results support the view that the preconception diet received by males and females differentially affects embryonic development.
Additional keywords: fetal programming, fish, polyunsaturated fatty acids, pouch function, reproduction.
References
Ahnesjö, I., and Craig, J. F. (2011). The biology of Syngnathidae: pipefishes, seadragons and seahorses. J. Fish Biol. 78, 1597–1602.| The biology of Syngnathidae: pipefishes, seadragons and seahorses.Crossref | GoogleScholarGoogle Scholar | 21651518PubMed |
Association of Official Analytical Chemists (AOAC). (2010). ‘Official methods of analysis of the Association of Official Analytical Chemists.’ (AOAC International: Washington, DC.)
Bateson, P., Gluckman, P., and Hanson, M. (2014). The biology of developmental plasticity and the predictive adaptive response hypothesis. J. Physiol. 592, 2357–2368.
| The biology of developmental plasticity and the predictive adaptive response hypothesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXovVWhu7k%3D&md5=40f65753727d4d5fe040c180d6c1aa9fCAS | 24882817PubMed |
Carcupino, M., Baldacci, A., Mazzini, M., and 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. J. Fish Biol. 61, 1465–1480.
| 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.Crossref | GoogleScholarGoogle Scholar |
Christie, W. W. (1982). ‘Lipid Analysis. 2nd Revised Edition.’ (Pergamon Press: Oxford.)
Fernandez, M. L., and West, K. L. (2005). Mechanisms by which dietary fatty acids modulate plasma lipids. J. Nutr. 135, 2075–2078.
| 1:CAS:528:DC%2BD2MXhtVSktbnJ&md5=937b0bedeb3346080a7b734577f5cd25CAS | 16140878PubMed |
Folch, J., Lees, M., and Sloane Stanley, G. H. (1957). A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226, 497–509.
| 1:STN:280:DyaG2s%2FnsFCjtw%3D%3D&md5=7af8b449eecca02927736f072881bbefCAS | 13428781PubMed |
Foster, S. J., and Vincent, A. C. J. (2004). Life history and ecology of seahorses: implications for conservation and management. J. Fish Biol. 65, 1–61.
| Life history and ecology of seahorses: implications for conservation and management.Crossref | GoogleScholarGoogle Scholar |
García-Manchón, J., Socorro-Cruz, J., Segade Botella, A., Otero-Ferrer, F., Mesa, A., and Molina-Domínguez, L. (2013). First feeding regimes for long-snout seahorse Hippocampus reidi larvae. Commun. Agric. Appl. Biol. Sci. 78, 139–142.
| 25141649PubMed |
Gemmell, B. J., Sheng, J., and Buskey, E. J. (2013). Morphology of seahorse head hydrodynamically aids in capture of evasive prey. Nat. Commun. 4, 2840.
| Morphology of seahorse head hydrodynamically aids in capture of evasive prey.Crossref | GoogleScholarGoogle Scholar | 24281430PubMed |
Gluckman, P. D., Hanson, M. A., and Beedle, A. S. (2007). Early life events and their consequences for later disease: a life history and evolutionary perspective. Am. J. Hum. Biol. 19, 1–19.
| Early life events and their consequences for later disease: a life history and evolutionary perspective.Crossref | GoogleScholarGoogle Scholar | 17160980PubMed |
Haresign, T. W., and Shumway, S. E. (1981). Permeability of the marsupium of the pipefish Syngnathus fuscus to [14C]-alpha amino isobutyric acid. Comp. Biochem. Physiol. Part A. Physiol. 69, 603–604.
| Permeability of the marsupium of the pipefish Syngnathus fuscus to [14C]-alpha amino isobutyric acid.Crossref | GoogleScholarGoogle Scholar |
Hora, M. S. C. d., and Joyeux, J.-C. (2009). Closing the reproductive cycle: growth of the seahorse Hippocampus reidi (Teleostei, Syngnathidae) from birth to adulthood under experimental conditions. Aquaculture 292, 37–41.
| Closing the reproductive cycle: growth of the seahorse Hippocampus reidi (Teleostei, Syngnathidae) from birth to adulthood under experimental conditions.Crossref | GoogleScholarGoogle Scholar |
Izquierdo, M., Watanabe, T., Takeuchi, T., Arakawa, T., and Kitajima, C. (1990). Optimum EFA levels in Artemia to meet the EFA requirements of red sea bream (Pagrus major). In ‘Status of Fish Nutrition in Aquaculture. Third International Symposium on Feeding and Nutrition in Fish.The Current Status of fish Nutrition in Aquaculture.’ (Eds M. Takeda and T. Watanabe.) pp. 221–232. (Japan Translation Center: Tokyo.)
Izquierdo, M. S., Fernández-Palacios, H., and Tacon, A. G. J. (2001). Effect of broodstock nutrition on reproductive performance of fish. Aquaculture 197, 25–42.
| Effect of broodstock nutrition on reproductive performance of fish.Crossref | GoogleScholarGoogle Scholar |
Kvarnemo, C., Mobley, K. B., Partridge, C., Jones, A. G., and Ahnesjo, I. (2011). Evidence of paternal nutrient provisioning to embryos in broad-nosed pipefish Syngnathus typhle. J. Fish Biol. 78, 1725–1737.
| Evidence of paternal nutrient provisioning to embryos in broad-nosed pipefish Syngnathus typhle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpvVWrtr8%3D&md5=9ab62b09d700b059359b6dad326ab824CAS | 21651524PubMed |
Lourie, S. A. (2003). Measuring seahorses. In ‘Project Seahorse. Technical Report Series 4.’ (Fisheries Centre, University of British Columbia: Vancouver.)
Mai, A. C. G., and Velasco, G. (2012). Population dynamics and reproduction of wild longsnout seahorse Hippocampus reidi. J. Mar. Biol. Assoc. U. K. 92, 421–427.
| Population dynamics and reproduction of wild longsnout seahorse Hippocampus reidi.Crossref | GoogleScholarGoogle Scholar |
Melamed, P., Xue, Y., Poon, J. F., Wu, Q., Xie, H., Yeo, J., Foo, T. W., and Chua, H. K. (2005). The male seahorse synthesizes and secretes a novel C-type lectin into the brood pouch during early pregnancy. FEBS J. 272, 1221–1235.
| The male seahorse synthesizes and secretes a novel C-type lectin into the brood pouch during early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXit12ru74%3D&md5=32c9ebde2fad78984f240d0718657d47CAS | 15720396PubMed |
Otero-Ferrer, F., Molina, L., Socorro, J., Herrera, R., Fernández-Palacios, H., and Soledad Izquierdo, M. (2010). Live prey first feeding regimes for short-snouted seahorse Hippocampus hippocampus (Linnaeus, 1758) juveniles. Aquacult. Res. 41, e8–e19.
| Live prey first feeding regimes for short-snouted seahorse Hippocampus hippocampus (Linnaeus, 1758) juveniles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlOqsLbP&md5=8a7b1bdce4c66ce6d1e346e0886302deCAS |
Otero-Ferrer, F., Molina, L., Socorro, J., Fernandez-Palacios, H., Izquierdo, M., and Herrera, R. (2012). Effect of different live prey on spawning quality of short-snouted seahorse, Hippocampus hippocampus (Linnaeus, 1758). J. World Aquacult. Soc. 43, 174–186.
| Effect of different live prey on spawning quality of short-snouted seahorse, Hippocampus hippocampus (Linnaeus, 1758).Crossref | GoogleScholarGoogle Scholar |
Paczolt, K. A., and Jones, A. G. (2010). Post-copulatory sexual selection and sexual conflict in the evolution of male pregnancy. Nature 464, 401–404.
| Post-copulatory sexual selection and sexual conflict in the evolution of male pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjsFSqtL4%3D&md5=fb26b3f13491b28ec3f8cb66f29f42f1CAS | 20237568PubMed |
Palma, J., Andrade, J. P., and Bureau, D. P. (2012). Growth, reproductive performances, and brood quality of long snout seahorse, Hippocampus guttulatus, fed enriched shrimp diets. J. World Aquacult. Soc. 43, 802–813.
| Growth, reproductive performances, and brood quality of long snout seahorse, Hippocampus guttulatus, fed enriched shrimp diets.Crossref | GoogleScholarGoogle Scholar |
Planas, M., Quintas, P., Chamorro, A., and Silva, C. (2010). Female maturation, egg characteristics and fatty acids profile in the seahorse Hippocampus guttulatus. Anim. Reprod. Sci. 122, 66–73.
| Female maturation, egg characteristics and fatty acids profile in the seahorse Hippocampus guttulatus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1Kqt7nK&md5=b834b7ad3c941b71e4b20b7b43ff6c3cCAS | 20727689PubMed |
Poortenaar, C. W., Woods, C. M. C., James, P. J., Giambartolomei, F. M., and Lokman, P. M. (2004). Reproductive biology of female big-bellied seahorses. J. Fish Biol. 64, 717–725.
| Reproductive biology of female big-bellied seahorses.Crossref | GoogleScholarGoogle Scholar |
Ripley, J. L., and 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.
| Direct evidence for embryonic uptake of paternally-derived nutrients in two pipefishes (Syngnathidae: Syngnathus spp.).Crossref | GoogleScholarGoogle Scholar | 19005657PubMed |
Roth, O., Klein, V., Beemelmanns, A., Scharsack, J. P., and Reusch, T. B. H. (2012). Male pregnancy and biparental immune priming. Am. Nat. 180, 802–814.
| Male pregnancy and biparental immune priming.Crossref | GoogleScholarGoogle Scholar | 23149404PubMed |
Saavedra, M., Masdeu, M., Hale, P., Sibbons, C. M., and Holt, W. V. (2014). Dietary fatty acid enrichment increases egg size and quality of yellow seahorse Hippocampus kuda. Anim. Reprod. Sci. 145, 54–61.
| Dietary fatty acid enrichment increases egg size and quality of yellow seahorse Hippocampus kuda.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFCjs73O&md5=fdde1c534f8e6749270e6ef0e501f8a2CAS | 24070584PubMed |
Sagebakken, G., Ahnesjo, I., Mobley, K. B., Braga Goncalves, I., and Kvarnemo, C. (2010). Brooding fathers, not siblings, take up nutrients from embryos. Proc. Biol. Sci. 277, 971–977.
| Brooding fathers, not siblings, take up nutrients from embryos.Crossref | GoogleScholarGoogle Scholar | 19939847PubMed |
Selman, K., Wallace, R. A., and Player, D. (1991). Ovary of the seahorse, Hippocampus erectus. J. Morphol. 209, 285–304.
| Ovary of the seahorse, Hippocampus erectus.Crossref | GoogleScholarGoogle Scholar |
Sogabe, A., Matsumoto, K., Ohashi, M., Watanabe, A., Takata, H., Murakami, Y., Omori, K., and Yanagisawa, Y. (2008). A monogamous pipefish has the same type of ovary as observed in monogamous seahorses. Biol. Lett. 4, 362–365.
| A monogamous pipefish has the same type of ovary as observed in monogamous seahorses.Crossref | GoogleScholarGoogle Scholar | 18492646PubMed |
Stölting, K. N., and Wilson, A. B. (2007). Male pregnancy in seahorses and pipefish: beyond the mammalian model. Bioessays 29, 884–896.
| Male pregnancy in seahorses and pipefish: beyond the mammalian model.Crossref | GoogleScholarGoogle Scholar | 17691105PubMed |
Van Wassenbergh, S., Leysen, H., Adriaens, D., and Aerts, P. (2013). Mechanics of snout expansion in suction-feeding seahorses: musculoskeletal force transmission. J. Exp. Biol. 216, 407–417.
| Mechanics of snout expansion in suction-feeding seahorses: musculoskeletal force transmission.Crossref | GoogleScholarGoogle Scholar | 23038729PubMed |
Zar, J. H. (1984). ‘Biostatistical Analysis.’ (Prentice Hall: Chicago.)