- Email: [email protected]
Imprinting: Seeing Food and Eating It
Dispatch R501
type of phototrophy in the sea. Science 289, 1902–1906. 10. Giovannoni, S.J., Bibbs, L., Cho, J.C., Stapels, M.D., Desiderio, R., Vergin, K.L., Rappe, M.S., Laney, S., Wilhelm, L.J., Tripp, H.J., et al. (2005). Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature 438, 82–85. 11. Beja, O., Spudich, E.N., Spudich, J.L., Leclerc, M., and DeLong, E.F. (2001). Proteorhodopsin phototrophy in the ocean. Nature 411, 786–789. 12. Thompson, J.R., Pacocha, S., Pharino, C., Klepac-Ceraj, V., Hunt, D.E., Benoit, J., Sarma-Rupavtarm, R., Distel, D.L., and Polz, M.F. (2005). Genotypic diversity within a natural coastal bacterioplankton population. Science 307, 1311–1313.
13. Kuypers, M.M., Sliekers, A.O., Lavik, G., Schmid, M., Jorgensen, B.B., Kuenen, J.G., Sinninghe Damste, J.S., Strous, M., and Jetten, M.S. (2003). Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422, 608–611. 14. Kuypers, M.M., Lavik, G., Woebken, D., Schmid, M., Fuchs, B.M., Amann, R., Jorgensen, B.B., and Jetten, M.S. (2005). Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc. Natl. Acad. Sci. USA 102, 6478–6483. 15. Ram, R.J., VerBerkmoes, N.C., Thelen, M.P., Tyson, G.W., Baker, B.J., Blake, R.C., Shah, M., Hettich, R.L., and Banfield, J.F. (2005). Community
Imprinting: Seeing Food and Eating It A recent study has found that although, ordinarily, cuttlefish hatchlings prefer shrimp-like prey, when visually exposed to crabs in the first hours of day one, they later prefer crabs to shrimps. As the development of this preference occurs during a short sensitive phase, does not depend on food ingestion and is long lasting, it fulfils all the criteria for imprinting, a phenomenon more usually associated with vertebrates and social learning. Susan D. Healy Early experiences in life can have a major impact on an animal’s behaviour. Sometimes the impact occurs almost immediately, sometimes it persists for a lifetime. When these experiences are acquired within a specified period of time (the ‘sensitive period’), have no obvious immediate reinforcement and last for a long time, they are considered to constitute a special kind of learning known as imprinting. In a recent study by Darmaillacq et al. [1], three-day old cuttlefish were found to prefer crabs over shrimps as a result of being visually exposed to crabs in the first few hours after hatching. Although early experience of particular foods influences subsequent food choice in a range of animals, even in humans (for example [2]), previous studies have either examined preferences after animals had ingested the test food (for example [3]), or not looked for the existence of a sensitive period (for example [4]). In this new study [1], cuttlefish that had hatched during the previous night were exposed to
small Carcinus crabs for between 15 and 120 minutes, during which time none of the crabs was consumed. On day three, the first day in which the hatchlings were provided with food (they usually do not eat before this time), they were offered both shrimps and crabs. Although some shrimps were eaten, the overwhelming preference was for crabs. However, this preference was dependent on two aspects of the early exposure: only those hatchlings that saw crabs within two hours after sunrise on their first day preferred crabs, compared with hatchlings exposed at 4 hours, or later, after sunrise; and only hatchlings that were exposed for 2 hours to crabs had a preference for crabs. Those hatchlings exposed to crabs for 15–60 minutes exhibited the usual innate preference for shrimp-like prey [5]. These preferences persisted for seven days and following consumption of shrimp. This kind of non-exclusive preference — three-day old hatchlings will eat shrimps, they simply prefer crabs — has similarities with sexual imprinting, in which juvenile animals develop
proteomics of a natural microbial biofilm. Science 308, 1915–1920. 16. Stapels, M.E., Cho, J.C., Giovannoni, S.J., and Barofsky, D.F. (2004). Proteomic analysis of novel marine bacteria using MALDI and ESI mass spectrometry. J. Biomol. Tech. 15, 191–198.
Department of Microbiology, Cornell University, Ithaca, New York 14853, USA. E-mail: [email protected]
DOI: 10.1016/j.cub.2006.06.007
preferences for mates based on the appearance and behaviour of, often, family members [6]. Young birds raised by parents of foster species often later choose mates from the foster species (leading to poor, or no, reproductive success), although they will mate with individuals from their own species if that is the only option. The lengthy duration of the food imprinting effect is also similar, although not to quite the same extent (as far as we know) as the effect on mate choice, which occurs months after the imprinting has occurred. Precocial animals, like domestic chicks and cuttlefish, which are independent within hours of hatch or birth and which receive no posthatch parental care have two options for acquisition of information: bring it into the world with you (unlearned preferences for food, sexual partners and so on) or pick up the information as you go (trial and error learning). Imprinting allows something in between: a certain degree of flexibility in response, useful for learning information for which the timing is likely to be predictable — food seen in first few hours of life, sibling/parents seen during juvenile stages — but in which specifying the exact details of the experience is not useful. Although food imprinting has previously attracted little attention, it seems that for animals such as cuttlefish there are clear advantages to learning the visual features of potential food items so as to deal with a world that is not filled with shrimp-like possibilities. What is less clear is
Current Biology Vol 16 No 13 R502
why such preferences should be long-lasting, if indeed they last longer than the seven days demonstrated by Darmaillacq et al. [1]. In both sexual and filial imprinting — animal imprints on features of mother or siblings [7] — the benefits to both the timing and duration of the imprinting are reasonably clear: life-long retention of the memories of the features of siblings will be useful for all mate choices so as to avoid inbreeding. Likewise, learning the adult features of members of your species so as to avoid mating with the wrong species will not become redundant, even as experience of mate choice (and with the outcomes of that choice) increases. Food imprinting, on the other hand, would seem less valuable in the long term. For any long-lived animal, in particular one living in even somewhat changeable environments, a durable food preference may even be costly. In humans, for example, food preferences developed during childhood may contribute to poor eating patterns in adulthood [8]. Understanding the role of learning mechanisms such as imprinting, and the importance of sensory and
social context on food preferences, may shed light on what appear to be inappropriate food choices and consumption patterns, for example, over-consumption of foods high in sugar and fat [9,10]. Finally, determining the existence of, and the context in which food imprinting occurs, across species will aid our understanding of the generality of learning mechanisms. There continues to be debate as to whether natural selection has shaped the occurrence or kind of learning abilities animals possess [11]. The discovery, for example, that not all animals imprint on food would contribute to the question of whether or not there are adaptive specialisations in cognition (for example [12])? References 1. Darmaillacq, A.S., Chichery, M.P., and Dickel, L. (2006). Food imprinting, new evidence from cuttlefish Sepia officinalis. Biol. Lett. FirstCite, 1–3. 2. Wansink, B. (2002). Changing eating habits on the home front: Lost lessons from World War II research. J. Pub. Pol. Market. 21, 90–99. 3. Punzo, F. (2002). Early experience and prey preference in the lynx spider, Oxyopes salticus Hentz (Araneae: Oxyopidae). J.N.Y. Ent. Soc. 110, 255–259. 4. Darmaillacq, A.S., Chichery, R., Shashar, N., and Dickel, L. (2006). Early
Left–Right Asymmetry: Actin– Myosin through the Looking Glass Despite being bilaterally symmetric, most Metazoa exhibit clear, genetically determined left–right differences. In several animals, microtubule-based structures are thought to be the source of chiral information used to establish handedness. Now, two new studies in Drosophila identify a role for unconventional myosin motors in this process. Buzz Baum ‘If events show a certain dissymmetry, the same dissymmetry should be revealed in their causes.’ Pierre Curie, 1894.
Although bilateral animals appear left–right (L–R) symmetric from the outside, their internal organs often exhibit stereotypical L–R differences in their position and morphology [1,2]. Our hearts, for
example, are usually on our left-hand side. Although it is still not clear how this difference between the left and right sides of embryos is specified, the process is known to be under genetic control [3]. Surprisingly, when genes required for L–R patterning were first cloned, several were found to code for components of tubulin-based cilia: including two microtubulebased motors [4,5], prompting the search for a causal link between
5.
6.
7. 8.
9.
10.
11.
12.
familiarization overrides innate prey preference in newly hatched Sepia officinalis cuttlefish. Anim. Behav. 71, 511–514. Darmaillacq, A.S., Chichery, R., Poirier, R., and Dickel, L. (2004). Effect of early feeding experience on subsequent prey preference by cuttlefish, Sepia officinalis. Devel. Psychobiol. 45, 239–244. ten Cate, C., and Vos, D.R. (1999). Sexual imprinting and evolutionary processes in birds: A reassessment. Adv. Stud. Behav. 28, 1–31. Lorenz, K. (1937). The companion in the bird’s world. Auk 54, 245–273. Cashdan, E. (1994). A sensitive period for learning about food. Hum. Nat. 5, 279–291. Cooke, L., Wardle, J., and Gibson, E.L. (2003). Relationship between parental report of food neophobia and everyday food consumption in 2-6-year-old children. Appetite 41, 205–206. Drewnowski, A. (1997). Taste preference and food intake. Annu. Rev. Nutrition 17, 237–253. Healy, S.D., de Kort, S.R., and Clayton, N.S. (2005). The hippocampus, spatial memory and food hoarding: a puzzle revisited. Trends Ecol. Evol. 20, 17–22. Ratcliffe, J.M., Fenton, M.B., and Galef, B.G. (2003). An exception to the rule: common vampire bats do not learn taste aversions. Anim. Behav. 65, 385–389.
Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3JT, UK. E-mail: [email protected]
DOI: 10.1016/j.cub.2006.06.013
cilia and L–R patterning. The results were spectacular: it was discovered that in the early mouse embryo, in a structure called ‘the node’, ordered rows of tilted cilia rotate in a clockwise direction to power a leftward flow of extracellular fluid [3]. As artificially reversing this flow is sufficient to reverse L–R symmetry [6], the cilia-based movement is likely to play a causal role in L–R symmetry breaking — perhaps through the establishment of a gradient of an extracellular signalling molecule or through mechanosensation [3]. Although the case in mouse is compelling, cilia do not appear to be at the right place and time to be involved in the establishment of handedness in a variety of other systems [7,8]. Hence the significance of the recent discovery of a role for myosin I motors in the regulation of handedness in the
type of phototrophy in the sea. Science 289, 1902–1906. 10. Giovannoni, S.J., Bibbs, L., Cho, J.C., Stapels, M.D., Desiderio, R., Vergin, K.L., Rappe, M.S., Laney, S., Wilhelm, L.J., Tripp, H.J., et al. (2005). Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature 438, 82–85. 11. Beja, O., Spudich, E.N., Spudich, J.L., Leclerc, M., and DeLong, E.F. (2001). Proteorhodopsin phototrophy in the ocean. Nature 411, 786–789. 12. Thompson, J.R., Pacocha, S., Pharino, C., Klepac-Ceraj, V., Hunt, D.E., Benoit, J., Sarma-Rupavtarm, R., Distel, D.L., and Polz, M.F. (2005). Genotypic diversity within a natural coastal bacterioplankton population. Science 307, 1311–1313.
13. Kuypers, M.M., Sliekers, A.O., Lavik, G., Schmid, M., Jorgensen, B.B., Kuenen, J.G., Sinninghe Damste, J.S., Strous, M., and Jetten, M.S. (2003). Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422, 608–611. 14. Kuypers, M.M., Lavik, G., Woebken, D., Schmid, M., Fuchs, B.M., Amann, R., Jorgensen, B.B., and Jetten, M.S. (2005). Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc. Natl. Acad. Sci. USA 102, 6478–6483. 15. Ram, R.J., VerBerkmoes, N.C., Thelen, M.P., Tyson, G.W., Baker, B.J., Blake, R.C., Shah, M., Hettich, R.L., and Banfield, J.F. (2005). Community
Imprinting: Seeing Food and Eating It A recent study has found that although, ordinarily, cuttlefish hatchlings prefer shrimp-like prey, when visually exposed to crabs in the first hours of day one, they later prefer crabs to shrimps. As the development of this preference occurs during a short sensitive phase, does not depend on food ingestion and is long lasting, it fulfils all the criteria for imprinting, a phenomenon more usually associated with vertebrates and social learning. Susan D. Healy Early experiences in life can have a major impact on an animal’s behaviour. Sometimes the impact occurs almost immediately, sometimes it persists for a lifetime. When these experiences are acquired within a specified period of time (the ‘sensitive period’), have no obvious immediate reinforcement and last for a long time, they are considered to constitute a special kind of learning known as imprinting. In a recent study by Darmaillacq et al. [1], three-day old cuttlefish were found to prefer crabs over shrimps as a result of being visually exposed to crabs in the first few hours after hatching. Although early experience of particular foods influences subsequent food choice in a range of animals, even in humans (for example [2]), previous studies have either examined preferences after animals had ingested the test food (for example [3]), or not looked for the existence of a sensitive period (for example [4]). In this new study [1], cuttlefish that had hatched during the previous night were exposed to
small Carcinus crabs for between 15 and 120 minutes, during which time none of the crabs was consumed. On day three, the first day in which the hatchlings were provided with food (they usually do not eat before this time), they were offered both shrimps and crabs. Although some shrimps were eaten, the overwhelming preference was for crabs. However, this preference was dependent on two aspects of the early exposure: only those hatchlings that saw crabs within two hours after sunrise on their first day preferred crabs, compared with hatchlings exposed at 4 hours, or later, after sunrise; and only hatchlings that were exposed for 2 hours to crabs had a preference for crabs. Those hatchlings exposed to crabs for 15–60 minutes exhibited the usual innate preference for shrimp-like prey [5]. These preferences persisted for seven days and following consumption of shrimp. This kind of non-exclusive preference — three-day old hatchlings will eat shrimps, they simply prefer crabs — has similarities with sexual imprinting, in which juvenile animals develop
proteomics of a natural microbial biofilm. Science 308, 1915–1920. 16. Stapels, M.E., Cho, J.C., Giovannoni, S.J., and Barofsky, D.F. (2004). Proteomic analysis of novel marine bacteria using MALDI and ESI mass spectrometry. J. Biomol. Tech. 15, 191–198.
Department of Microbiology, Cornell University, Ithaca, New York 14853, USA. E-mail: [email protected]
DOI: 10.1016/j.cub.2006.06.007
preferences for mates based on the appearance and behaviour of, often, family members [6]. Young birds raised by parents of foster species often later choose mates from the foster species (leading to poor, or no, reproductive success), although they will mate with individuals from their own species if that is the only option. The lengthy duration of the food imprinting effect is also similar, although not to quite the same extent (as far as we know) as the effect on mate choice, which occurs months after the imprinting has occurred. Precocial animals, like domestic chicks and cuttlefish, which are independent within hours of hatch or birth and which receive no posthatch parental care have two options for acquisition of information: bring it into the world with you (unlearned preferences for food, sexual partners and so on) or pick up the information as you go (trial and error learning). Imprinting allows something in between: a certain degree of flexibility in response, useful for learning information for which the timing is likely to be predictable — food seen in first few hours of life, sibling/parents seen during juvenile stages — but in which specifying the exact details of the experience is not useful. Although food imprinting has previously attracted little attention, it seems that for animals such as cuttlefish there are clear advantages to learning the visual features of potential food items so as to deal with a world that is not filled with shrimp-like possibilities. What is less clear is
Current Biology Vol 16 No 13 R502
why such preferences should be long-lasting, if indeed they last longer than the seven days demonstrated by Darmaillacq et al. [1]. In both sexual and filial imprinting — animal imprints on features of mother or siblings [7] — the benefits to both the timing and duration of the imprinting are reasonably clear: life-long retention of the memories of the features of siblings will be useful for all mate choices so as to avoid inbreeding. Likewise, learning the adult features of members of your species so as to avoid mating with the wrong species will not become redundant, even as experience of mate choice (and with the outcomes of that choice) increases. Food imprinting, on the other hand, would seem less valuable in the long term. For any long-lived animal, in particular one living in even somewhat changeable environments, a durable food preference may even be costly. In humans, for example, food preferences developed during childhood may contribute to poor eating patterns in adulthood [8]. Understanding the role of learning mechanisms such as imprinting, and the importance of sensory and
social context on food preferences, may shed light on what appear to be inappropriate food choices and consumption patterns, for example, over-consumption of foods high in sugar and fat [9,10]. Finally, determining the existence of, and the context in which food imprinting occurs, across species will aid our understanding of the generality of learning mechanisms. There continues to be debate as to whether natural selection has shaped the occurrence or kind of learning abilities animals possess [11]. The discovery, for example, that not all animals imprint on food would contribute to the question of whether or not there are adaptive specialisations in cognition (for example [12])? References 1. Darmaillacq, A.S., Chichery, M.P., and Dickel, L. (2006). Food imprinting, new evidence from cuttlefish Sepia officinalis. Biol. Lett. FirstCite, 1–3. 2. Wansink, B. (2002). Changing eating habits on the home front: Lost lessons from World War II research. J. Pub. Pol. Market. 21, 90–99. 3. Punzo, F. (2002). Early experience and prey preference in the lynx spider, Oxyopes salticus Hentz (Araneae: Oxyopidae). J.N.Y. Ent. Soc. 110, 255–259. 4. Darmaillacq, A.S., Chichery, R., Shashar, N., and Dickel, L. (2006). Early
Left–Right Asymmetry: Actin– Myosin through the Looking Glass Despite being bilaterally symmetric, most Metazoa exhibit clear, genetically determined left–right differences. In several animals, microtubule-based structures are thought to be the source of chiral information used to establish handedness. Now, two new studies in Drosophila identify a role for unconventional myosin motors in this process. Buzz Baum ‘If events show a certain dissymmetry, the same dissymmetry should be revealed in their causes.’ Pierre Curie, 1894.
Although bilateral animals appear left–right (L–R) symmetric from the outside, their internal organs often exhibit stereotypical L–R differences in their position and morphology [1,2]. Our hearts, for
example, are usually on our left-hand side. Although it is still not clear how this difference between the left and right sides of embryos is specified, the process is known to be under genetic control [3]. Surprisingly, when genes required for L–R patterning were first cloned, several were found to code for components of tubulin-based cilia: including two microtubulebased motors [4,5], prompting the search for a causal link between
5.
6.
7. 8.
9.
10.
11.
12.
familiarization overrides innate prey preference in newly hatched Sepia officinalis cuttlefish. Anim. Behav. 71, 511–514. Darmaillacq, A.S., Chichery, R., Poirier, R., and Dickel, L. (2004). Effect of early feeding experience on subsequent prey preference by cuttlefish, Sepia officinalis. Devel. Psychobiol. 45, 239–244. ten Cate, C., and Vos, D.R. (1999). Sexual imprinting and evolutionary processes in birds: A reassessment. Adv. Stud. Behav. 28, 1–31. Lorenz, K. (1937). The companion in the bird’s world. Auk 54, 245–273. Cashdan, E. (1994). A sensitive period for learning about food. Hum. Nat. 5, 279–291. Cooke, L., Wardle, J., and Gibson, E.L. (2003). Relationship between parental report of food neophobia and everyday food consumption in 2-6-year-old children. Appetite 41, 205–206. Drewnowski, A. (1997). Taste preference and food intake. Annu. Rev. Nutrition 17, 237–253. Healy, S.D., de Kort, S.R., and Clayton, N.S. (2005). The hippocampus, spatial memory and food hoarding: a puzzle revisited. Trends Ecol. Evol. 20, 17–22. Ratcliffe, J.M., Fenton, M.B., and Galef, B.G. (2003). An exception to the rule: common vampire bats do not learn taste aversions. Anim. Behav. 65, 385–389.
Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3JT, UK. E-mail: [email protected]
DOI: 10.1016/j.cub.2006.06.013
cilia and L–R patterning. The results were spectacular: it was discovered that in the early mouse embryo, in a structure called ‘the node’, ordered rows of tilted cilia rotate in a clockwise direction to power a leftward flow of extracellular fluid [3]. As artificially reversing this flow is sufficient to reverse L–R symmetry [6], the cilia-based movement is likely to play a causal role in L–R symmetry breaking — perhaps through the establishment of a gradient of an extracellular signalling molecule or through mechanosensation [3]. Although the case in mouse is compelling, cilia do not appear to be at the right place and time to be involved in the establishment of handedness in a variety of other systems [7,8]. Hence the significance of the recent discovery of a role for myosin I motors in the regulation of handedness in the