- Email: [email protected]
Stereotypical resting behavior of the sperm whale
Magazine R21
Figure 3. A partly bleached coral. The coral is still alive, but the polyps in the bleached parts have lost their symbiotic algae. Photo courtesy of David Kline.
Correspondences
Stereotypical resting behavior of the sperm whale Patrick J.O. Miller1, Kagari Aoki2, Luke E. Rendell1 and Masao Amano3
by side. Conservation measures must thus work to ensure that on balance growth outpaces destruction, and that the natural ability of reefs to recover from disturbance (‘resilience’) is maintained. To date, marine protected areas have been the focus of most attention. Conspicuous successes include placing about one third of the Great Barrier Reef in no-take zones, and protection of the Northwest Hawaiian Islands. Marine protected areas do result in the rebound of most fish populations, and although documentation of the positive effects on corals is as yet more limited, there are promising signs. However, globally less than 2% of coral reefs are largely protected from fishing, and even these are often threatened by poor water quality. Moreover, localized protection alone cannot save reefs. In developing countries, traditional management schemes may be more effective given socio-economic constraints, and management of reefs outside marine protected areas is also clearly critical, with improved land-use and protection of herbivores being top priorities. Techniques for restoring reefs are being developed, but they are necessarily small in scale and expensive, and will only work if the original causes of decline have ended. Given that even the best scenarios for reducing CO2 emissions suggest substantial and rapid deterioration of the physical environment, improvement in local conditions coupled with action to reduce global threats are essential if reefs are to survive into the next century.
Protecting and restoring these ecosystems are thus among today’s biggest environmental challenges. Reefs are not only of scientific interest — they provide many ecosystem services and are critical components of the economies of many (mostly developing) countries — tourism, fisheries, and coastal protection being the most prominent. Success will depend on collaborations between natural and social scientists — we need to know not only what kills coral reefs, but also their economic value to people. Further reading Baker, A. (2003). Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Ann. Rev. Ecol. Evol. Syst. 34, 661–689. Cinner, J.E., and Aswani, S. (2007). Integrating customary management into marine conservation. Biol. Conser. 140, 201–216. Dornelas, M., Connolly, S.R., and Hughes, T. P. (2006). Coral reef diversity refutes the neutral theory of biodiversity. Nature 440, 80–82. Harvel, D., Jordán-Dahlgren, E., Merkel, S., Rosenberg, E., Raymundo, L., Smith, G., Weil, E., and Willis, B. (2007). Coral disease, environmental drivers, and the balance between coral and microbial associates. Oceanography 20, 58–81. Hoegh-Guldberg, O. et al. (2007). The carbon crisis: coral reefs under rapid climate change and ocean acidification. Science, in press. Jackson, J.B.C. (1997). Reefs since Columbus. Coral Reefs 16 (Suppl.), S23–S32. Knowlton, N. (2001). The future of coral reefs. Proc. Natl. Acad. Sci. 98, 5419–5425. Mumby, P.J., Hastings, A., and Edwards, H.J. (2007). Thresholds and the resilience of Caribbean coral reefs. Nature 450, 98–100. Wood, R. (1999). Reef Evolution. (Oxford: Oxford University Press). Sale, P.F. (2002). Coral Reef Fishes: Dynamics and Diversity in a Complex Ecosystem (San Diego: Academic Press).
Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, MRC 163, PO Box 37012, Washington, DC 20013-7012, USA. Email: [email protected]
Though very little is known about sleep in wild cetaceans, toothed cetaceans in captivity sleep with one side of their brain at a time [1]. Such uni-hemispheric sleep is thought to enable swimming, voluntary breathing, predator avoidance and/or social contact during sleep at sea [2,3]. Using suction cup tags, we discovered that sperm whales (Physeter macrocephalus) worldwide conduct passive shallow ‘drift- dives’ in stereotypical vertical postures just below the sea surface. Bouts of drift-dives accounted for 7.1% of recording time, or 36.7% of non-foraging time. Drift-dives were weakly diurnal, occurring least from 06:00– 12:00 (3% of records), and most from 18:00–24:00 (30% of records). A group of vertically drifting whales were atypically non– responsive to a closely- passing vessel until it inadvertently touched them, suggesting that sperm whales might sleep during these stereotypical resting dives. We measured the underwater activity level of 59 sperm whales worldwide using data-logging tags attached with suction cups for a total of 562.9 hours (see Supplemental data available on-line with this issue for further details). Predominantly (80.6% of time), tagged whales conducted foraging dive bouts, which differ from non- foraging shallow dives (19.4% of time) in depth or the presence of echolocation clicks [4]. Although it has been suggested that sperm whales may rest at depth [5], we found that they swam steadily, or continually produced clicks during deep dives. Instead we discovered that 31 of 59 whales across all tagging locations conducted inactive
Current Biology Vol 18 No 1 R22
Figure 1. Behavioral sequence of a whale showing the two stereotypical forms of drift-dives made by sperm whales worldwide. The whale was tagged in the Gulf of Mexico in 2003 with a Dtag using suction cups [4]. In ‘head-up’ driftdives, the posterior end of the whale slowly sinks from a horizontal posture and the pitch of the whale (measured using accelerometers in the tags) increases. The fact that the posterior end of the whale submerges during passive drifting indicates that some activity is required for sperm whales to remain horizontal at the sea surface. In ‘head-down’ drift-dives, the whale first descends and remains for some time at ~1–2 animal lengths depth, head down, before passively, turning head-up. The upward flip is driven by centre-of-gravity buoyancy forces within the sperm whale. Sperm whale tissues are overall more dense than seawater [4], but less-dense oils within the large spermaceti organ and air within respiratory tracts are located in the anterior portion of the body. Bubbles were often released after whales flipped head-up, possibly to reduce positive buoyancy and thereby remain deeper in the water [4].
shallow dives (‘drift-dives’), with inactive durations ranging from 0.7-31.5 min (mean: 12.7 ± 8.7 s. d., N = 70), with surfacing times of 7.7 ± 6.0 min between them. Bouts of drift-dives had highly variable durations, ranging from 0.7- 233.5 min (quartiles: 3.7, 8.1, 38.7 min). Logistic regression showed that drift-dives were more likely to be present in longer records (t57 = 2.19, p = 0.029), indicating that some tag deployments were too short to record this rare behavior. Drift- dives had two forms depending on how they were initiated by the whale (Figure 1). Maximum tag depth was greater during ‘head-down’
(16.5 ± 4.9 m) versus ‘head-up’ (8.6 ± 4.8 m) drift-dives (t4 = 5.81, P < 0.001), though duration did not differ significantly (‘head-up’: 11.8 ± 9.2 min; ‘head- down’: 13.4 ± 8.7 min; t48 = 0.63, P = 0.54). It is unclear why sperm whales have two forms of resting dives, but the greater depth attained during ‘head-down’ dives may provide more stability for a whale resting at sea. The vertical drifting posture recorded by the tags matches that of whales occasionally observed at sea (Figure 2). In an opportunistic experiment, video was recorded from R/V Balaena as it approached a group of 12–13 whales under sail
Figure 2. Video frame showing three vertically drifting sperm whales passed within a few meters by R/V Balaena on 31 October 2000 off Northern Chile. The vessel approached slowly with engines off from the left prior to this frame and continued moving to the right following this frame (blue arrow). The red arrows indicate the mid-line axes of the bodies of the drifting whales. Note that the whales on the left and right had visibility of the vessel with the right eye prior to this frame, and then with the left eye as the vessel passed. The whale in the centre was slightly off-axis so the right eye may not have had visibility of the vessel (see Supplemental movie for entire sequence).
alone (see Supplemental movie). Six whales can clearly be seen to be motionless in a vertical posture with the head at or just below the sea surface. Three vertical whales were unusually non-responsive to the very close (<2 m) approach of the vessel, reacting only when unintentionally touched by the vessel, after which the entire group moved away. In contrast, a horizontally logging whale in the group reacted to the vessel at ~8 m distance. Our study reveals that sperm whales worldwide rest in a stereotypical fashion by drifting vertically under the sea surface. Sleep in captive cetaceans is usually studied using EEG or inspection of eye state, not feasible with large wild cetaceans. However, inactivity and stereotypical posture are two criteria of behavioral sleep in mammals. Lack of a response to the unusually close vessel approach until they were touched in the one instance we observed indicate that the final two criteria: elevated response thresholds and rapidly reversibility to wakefulness with sufficient stimulation [6] may also be met. More data are needed to confirm that the whales did not respond for other reasons, but we can hypothesize that sperm whales might conduct drift-dives in order to sleep. Drift-dive bouts accounted for 7.1% of the tag records, which would be less sleep than any other mammal studied [2,6]. However, the cetacean adaptation for uni- hemispheric sleep may enable sperm whales to sleep during other low-level activities such as ascent from depth [4] and surfacing-time during which whales voluntary breathe, interact socially, and perform movements to remain horizontal (Figure 1). Drift dives are a lower-activity state, though, and we propose that it could benefit sperm whales to take advantage of more-efficient bi-hemispheric sleep during drift-dives, as do phocid seals [3,7]. Interestingly, two drifting whales did not react to the vessel approach, though it passed across the field of vision of both eyes (Figure 2), consistent with bi-hemispheric sleep [8]. However, in contrast to captive birds and otariid seals
Magazine R23
which sleep uni-hemispherically or bi-hemispherically depending on the context [3], captive cetaceans almost never sleep bilaterally [1,8,9] even when they are motionless [10]. Unraveling how marine mammals manage the inherent tradeoff [3] between wakefulness and sleep will require the development of procedures for observing eye closure and other physiological variables, including EEG, in free-ranging animals. Supplemental data Supplemental data are available at http:// www.current-biology.com/cgi/content/ full/18/1/R21/DC1 References 1. Mukhametov, L.M., Supin, A.Y., and Polyakova, I.G. (1977). Interhemispheric asymmetry of the electrocephalographic sleep patterns in dolphins. Brain Res. 134, 581–584. 2. Siegel, J.M. (2005). Clues to the functions of mammalian sleep. Nature 437, 1264–1271. 3. Rattenborg, N.C., Amlaner, C.J., and Lima, S.L. (2000). Behavioral, neurophysiological and evolutionary perspectives on unihemispheric sleep. Neurosci. Biobehav. Rev. 24, 817–842. 4. Miller, P.J.O., Johnson, M.P., Tyack, P.L., and Terray, E.A. (2004). Swimming gaits, passive drag and buoyancy of diving sperm whales Physeter macrocephalus. J. Exp. Biol. 207, 1953–1967. 5. Amano, M., and Yoshioka, M. (2003). Sperm whale diving behavior monitored using a suction-cup-attached TDR tag. Marine Ecol. Prog. Ser. 258, 291–295. 6. Campbell, S.S., and Tobler, I. (1984). Animal sleep: a review of sleep duration across phylogeny. Neurosci. Biobehav. Rev. 8, 269–300. 7. Crocker, D.E., LeBoeuf, B.J., and Costa, D.P. (1997). Drift diving in female northern elephant seals: implications for food processing. Can. J. Zool. 75, 27–39. 8. Lyamin, O.I., Mukhametov, L.M., Siegel, J.M., Nazarenko, E.A., Polyakova, I.G., and Shpak, O.V. (2002). Unihemispheric slow wave sleep and the state of the eyes in a white whale. Behav. Brain Res. 129, 125–129. 9. Ridgway, S.H. (2002). Asymmetry and symmetry in brain waves from dolphin left and right hemispheres: some observations after anesthesia, during quiescent hanging behaviour, and during visual obstruction. Brain Behav. Evol. 60, 265–274. 10. Lyamin, O.I., Pryaslova, J., Kosenko, P., and Siegel, J. (2007). Behavioural aspects of sleep in bottlenose dolphin mothers and their calves. Physiol. Behav. doi:10.1016/j.physbeh.2007.05.064 1Sea
Mammal Research Unit, School of Biology, University of St. Andrews, Fife, KY16 8LB, UK. 2Ocean Research Institute, The University of Tokyo, 1-15-1 Minamidai, Nakano, Tokyo 164-8639, Japan. 3Department of Animal Sciences, Teikyo University of Science and Technology, 2525 Yatsuzawa, Uenohara, Yamanashi 409-0193, Japan. E-mail: [email protected]
Restoring sight in blind cavefish Richard Borowsky Twenty-nine populations of the blind cavefish, Astyanax mexicanus, are known from different caves in North-Eastern Mexico (Figure 1). They evolved from eyed, surface-dwelling forms which only reached the area in the mid-Pleistocene [1]. Quantitative genetic analyses have shown that the evolutionary impairment of eye development — as well as the loss of pigmentation and other cave-related changes — results from mutations at multiple gene sites (‘eye loci’) [2,3]. Eye loss has evolved independently at least three times [4,5] and at least some of the eye loci involved differ between the different cave populations [3]. Hybrids between blind cavefish from different caves have larger and better developed eye rudiments than their parents (Figure 2) [6], reflecting these independent origins and complementation [3,7,8]. Given the large number of mutations at different loci that have accumulated in these populations, we reasoned that hybridization among independently evolved populations might restore visual function. Here we demonstrate restoration of vision in cavefish Figure 1. Map of NorthEastern Mexico indicating locations of the cave populations studied. Molino and Pachón are 53 km distant and located in different drainages. Pachón and Tinaja are over 60 km distant and also in different drainages, while the Tinaja and Curva caves are only 12 km distant and in the same drainage.
whose immediate ancestors were blind and whose separate lineages may not have been exposed to light for the last one million years. We generated numerous F1 and F2 hybrid crosses among cave populations to test whether hybrids could see, and to elucidate the underlying genetics. Purebred cave and surface fish served as controls. We also created compound hybrids by crossing F1 surface/caveA hybrids with F1 surface/caveB hybrids. Eye regression progresses with age [7], so we studied fry (9 to 40 days old), to have the best chance of detecting vision. We measured body length and eye size and tested for vision using the optokinetic response: the reflexive following of moving stripes by the subject’s eyes [9]. Purebred cavefish from Molino, Pachón and Tinaja caves were tested for their optokinetic response (Supplemental data) and/or evidence of a dorsal light reflex, visual orientation to food items or response to a looming dark object. All cavefish were blind, consistent with the observation of serious defects in both lens and retinal structure during ‘Stage III’ of eye development [7]. Quantitative trait loci (QTL) studies identified at least twelve unlinked eye loci in Pachón cavefish [2]. For purposes of discussion only, we take this number to be typical of
Figure 3. A partly bleached coral. The coral is still alive, but the polyps in the bleached parts have lost their symbiotic algae. Photo courtesy of David Kline.
Correspondences
Stereotypical resting behavior of the sperm whale Patrick J.O. Miller1, Kagari Aoki2, Luke E. Rendell1 and Masao Amano3
by side. Conservation measures must thus work to ensure that on balance growth outpaces destruction, and that the natural ability of reefs to recover from disturbance (‘resilience’) is maintained. To date, marine protected areas have been the focus of most attention. Conspicuous successes include placing about one third of the Great Barrier Reef in no-take zones, and protection of the Northwest Hawaiian Islands. Marine protected areas do result in the rebound of most fish populations, and although documentation of the positive effects on corals is as yet more limited, there are promising signs. However, globally less than 2% of coral reefs are largely protected from fishing, and even these are often threatened by poor water quality. Moreover, localized protection alone cannot save reefs. In developing countries, traditional management schemes may be more effective given socio-economic constraints, and management of reefs outside marine protected areas is also clearly critical, with improved land-use and protection of herbivores being top priorities. Techniques for restoring reefs are being developed, but they are necessarily small in scale and expensive, and will only work if the original causes of decline have ended. Given that even the best scenarios for reducing CO2 emissions suggest substantial and rapid deterioration of the physical environment, improvement in local conditions coupled with action to reduce global threats are essential if reefs are to survive into the next century.
Protecting and restoring these ecosystems are thus among today’s biggest environmental challenges. Reefs are not only of scientific interest — they provide many ecosystem services and are critical components of the economies of many (mostly developing) countries — tourism, fisheries, and coastal protection being the most prominent. Success will depend on collaborations between natural and social scientists — we need to know not only what kills coral reefs, but also their economic value to people. Further reading Baker, A. (2003). Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Ann. Rev. Ecol. Evol. Syst. 34, 661–689. Cinner, J.E., and Aswani, S. (2007). Integrating customary management into marine conservation. Biol. Conser. 140, 201–216. Dornelas, M., Connolly, S.R., and Hughes, T. P. (2006). Coral reef diversity refutes the neutral theory of biodiversity. Nature 440, 80–82. Harvel, D., Jordán-Dahlgren, E., Merkel, S., Rosenberg, E., Raymundo, L., Smith, G., Weil, E., and Willis, B. (2007). Coral disease, environmental drivers, and the balance between coral and microbial associates. Oceanography 20, 58–81. Hoegh-Guldberg, O. et al. (2007). The carbon crisis: coral reefs under rapid climate change and ocean acidification. Science, in press. Jackson, J.B.C. (1997). Reefs since Columbus. Coral Reefs 16 (Suppl.), S23–S32. Knowlton, N. (2001). The future of coral reefs. Proc. Natl. Acad. Sci. 98, 5419–5425. Mumby, P.J., Hastings, A., and Edwards, H.J. (2007). Thresholds and the resilience of Caribbean coral reefs. Nature 450, 98–100. Wood, R. (1999). Reef Evolution. (Oxford: Oxford University Press). Sale, P.F. (2002). Coral Reef Fishes: Dynamics and Diversity in a Complex Ecosystem (San Diego: Academic Press).
Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, MRC 163, PO Box 37012, Washington, DC 20013-7012, USA. Email: [email protected]
Though very little is known about sleep in wild cetaceans, toothed cetaceans in captivity sleep with one side of their brain at a time [1]. Such uni-hemispheric sleep is thought to enable swimming, voluntary breathing, predator avoidance and/or social contact during sleep at sea [2,3]. Using suction cup tags, we discovered that sperm whales (Physeter macrocephalus) worldwide conduct passive shallow ‘drift- dives’ in stereotypical vertical postures just below the sea surface. Bouts of drift-dives accounted for 7.1% of recording time, or 36.7% of non-foraging time. Drift-dives were weakly diurnal, occurring least from 06:00– 12:00 (3% of records), and most from 18:00–24:00 (30% of records). A group of vertically drifting whales were atypically non– responsive to a closely- passing vessel until it inadvertently touched them, suggesting that sperm whales might sleep during these stereotypical resting dives. We measured the underwater activity level of 59 sperm whales worldwide using data-logging tags attached with suction cups for a total of 562.9 hours (see Supplemental data available on-line with this issue for further details). Predominantly (80.6% of time), tagged whales conducted foraging dive bouts, which differ from non- foraging shallow dives (19.4% of time) in depth or the presence of echolocation clicks [4]. Although it has been suggested that sperm whales may rest at depth [5], we found that they swam steadily, or continually produced clicks during deep dives. Instead we discovered that 31 of 59 whales across all tagging locations conducted inactive
Current Biology Vol 18 No 1 R22
Figure 1. Behavioral sequence of a whale showing the two stereotypical forms of drift-dives made by sperm whales worldwide. The whale was tagged in the Gulf of Mexico in 2003 with a Dtag using suction cups [4]. In ‘head-up’ driftdives, the posterior end of the whale slowly sinks from a horizontal posture and the pitch of the whale (measured using accelerometers in the tags) increases. The fact that the posterior end of the whale submerges during passive drifting indicates that some activity is required for sperm whales to remain horizontal at the sea surface. In ‘head-down’ drift-dives, the whale first descends and remains for some time at ~1–2 animal lengths depth, head down, before passively, turning head-up. The upward flip is driven by centre-of-gravity buoyancy forces within the sperm whale. Sperm whale tissues are overall more dense than seawater [4], but less-dense oils within the large spermaceti organ and air within respiratory tracts are located in the anterior portion of the body. Bubbles were often released after whales flipped head-up, possibly to reduce positive buoyancy and thereby remain deeper in the water [4].
shallow dives (‘drift-dives’), with inactive durations ranging from 0.7-31.5 min (mean: 12.7 ± 8.7 s. d., N = 70), with surfacing times of 7.7 ± 6.0 min between them. Bouts of drift-dives had highly variable durations, ranging from 0.7- 233.5 min (quartiles: 3.7, 8.1, 38.7 min). Logistic regression showed that drift-dives were more likely to be present in longer records (t57 = 2.19, p = 0.029), indicating that some tag deployments were too short to record this rare behavior. Drift- dives had two forms depending on how they were initiated by the whale (Figure 1). Maximum tag depth was greater during ‘head-down’
(16.5 ± 4.9 m) versus ‘head-up’ (8.6 ± 4.8 m) drift-dives (t4 = 5.81, P < 0.001), though duration did not differ significantly (‘head-up’: 11.8 ± 9.2 min; ‘head- down’: 13.4 ± 8.7 min; t48 = 0.63, P = 0.54). It is unclear why sperm whales have two forms of resting dives, but the greater depth attained during ‘head-down’ dives may provide more stability for a whale resting at sea. The vertical drifting posture recorded by the tags matches that of whales occasionally observed at sea (Figure 2). In an opportunistic experiment, video was recorded from R/V Balaena as it approached a group of 12–13 whales under sail
Figure 2. Video frame showing three vertically drifting sperm whales passed within a few meters by R/V Balaena on 31 October 2000 off Northern Chile. The vessel approached slowly with engines off from the left prior to this frame and continued moving to the right following this frame (blue arrow). The red arrows indicate the mid-line axes of the bodies of the drifting whales. Note that the whales on the left and right had visibility of the vessel with the right eye prior to this frame, and then with the left eye as the vessel passed. The whale in the centre was slightly off-axis so the right eye may not have had visibility of the vessel (see Supplemental movie for entire sequence).
alone (see Supplemental movie). Six whales can clearly be seen to be motionless in a vertical posture with the head at or just below the sea surface. Three vertical whales were unusually non-responsive to the very close (<2 m) approach of the vessel, reacting only when unintentionally touched by the vessel, after which the entire group moved away. In contrast, a horizontally logging whale in the group reacted to the vessel at ~8 m distance. Our study reveals that sperm whales worldwide rest in a stereotypical fashion by drifting vertically under the sea surface. Sleep in captive cetaceans is usually studied using EEG or inspection of eye state, not feasible with large wild cetaceans. However, inactivity and stereotypical posture are two criteria of behavioral sleep in mammals. Lack of a response to the unusually close vessel approach until they were touched in the one instance we observed indicate that the final two criteria: elevated response thresholds and rapidly reversibility to wakefulness with sufficient stimulation [6] may also be met. More data are needed to confirm that the whales did not respond for other reasons, but we can hypothesize that sperm whales might conduct drift-dives in order to sleep. Drift-dive bouts accounted for 7.1% of the tag records, which would be less sleep than any other mammal studied [2,6]. However, the cetacean adaptation for uni- hemispheric sleep may enable sperm whales to sleep during other low-level activities such as ascent from depth [4] and surfacing-time during which whales voluntary breathe, interact socially, and perform movements to remain horizontal (Figure 1). Drift dives are a lower-activity state, though, and we propose that it could benefit sperm whales to take advantage of more-efficient bi-hemispheric sleep during drift-dives, as do phocid seals [3,7]. Interestingly, two drifting whales did not react to the vessel approach, though it passed across the field of vision of both eyes (Figure 2), consistent with bi-hemispheric sleep [8]. However, in contrast to captive birds and otariid seals
Magazine R23
which sleep uni-hemispherically or bi-hemispherically depending on the context [3], captive cetaceans almost never sleep bilaterally [1,8,9] even when they are motionless [10]. Unraveling how marine mammals manage the inherent tradeoff [3] between wakefulness and sleep will require the development of procedures for observing eye closure and other physiological variables, including EEG, in free-ranging animals. Supplemental data Supplemental data are available at http:// www.current-biology.com/cgi/content/ full/18/1/R21/DC1 References 1. Mukhametov, L.M., Supin, A.Y., and Polyakova, I.G. (1977). Interhemispheric asymmetry of the electrocephalographic sleep patterns in dolphins. Brain Res. 134, 581–584. 2. Siegel, J.M. (2005). Clues to the functions of mammalian sleep. Nature 437, 1264–1271. 3. Rattenborg, N.C., Amlaner, C.J., and Lima, S.L. (2000). Behavioral, neurophysiological and evolutionary perspectives on unihemispheric sleep. Neurosci. Biobehav. Rev. 24, 817–842. 4. Miller, P.J.O., Johnson, M.P., Tyack, P.L., and Terray, E.A. (2004). Swimming gaits, passive drag and buoyancy of diving sperm whales Physeter macrocephalus. J. Exp. Biol. 207, 1953–1967. 5. Amano, M., and Yoshioka, M. (2003). Sperm whale diving behavior monitored using a suction-cup-attached TDR tag. Marine Ecol. Prog. Ser. 258, 291–295. 6. Campbell, S.S., and Tobler, I. (1984). Animal sleep: a review of sleep duration across phylogeny. Neurosci. Biobehav. Rev. 8, 269–300. 7. Crocker, D.E., LeBoeuf, B.J., and Costa, D.P. (1997). Drift diving in female northern elephant seals: implications for food processing. Can. J. Zool. 75, 27–39. 8. Lyamin, O.I., Mukhametov, L.M., Siegel, J.M., Nazarenko, E.A., Polyakova, I.G., and Shpak, O.V. (2002). Unihemispheric slow wave sleep and the state of the eyes in a white whale. Behav. Brain Res. 129, 125–129. 9. Ridgway, S.H. (2002). Asymmetry and symmetry in brain waves from dolphin left and right hemispheres: some observations after anesthesia, during quiescent hanging behaviour, and during visual obstruction. Brain Behav. Evol. 60, 265–274. 10. Lyamin, O.I., Pryaslova, J., Kosenko, P., and Siegel, J. (2007). Behavioural aspects of sleep in bottlenose dolphin mothers and their calves. Physiol. Behav. doi:10.1016/j.physbeh.2007.05.064 1Sea
Mammal Research Unit, School of Biology, University of St. Andrews, Fife, KY16 8LB, UK. 2Ocean Research Institute, The University of Tokyo, 1-15-1 Minamidai, Nakano, Tokyo 164-8639, Japan. 3Department of Animal Sciences, Teikyo University of Science and Technology, 2525 Yatsuzawa, Uenohara, Yamanashi 409-0193, Japan. E-mail: [email protected]
Restoring sight in blind cavefish Richard Borowsky Twenty-nine populations of the blind cavefish, Astyanax mexicanus, are known from different caves in North-Eastern Mexico (Figure 1). They evolved from eyed, surface-dwelling forms which only reached the area in the mid-Pleistocene [1]. Quantitative genetic analyses have shown that the evolutionary impairment of eye development — as well as the loss of pigmentation and other cave-related changes — results from mutations at multiple gene sites (‘eye loci’) [2,3]. Eye loss has evolved independently at least three times [4,5] and at least some of the eye loci involved differ between the different cave populations [3]. Hybrids between blind cavefish from different caves have larger and better developed eye rudiments than their parents (Figure 2) [6], reflecting these independent origins and complementation [3,7,8]. Given the large number of mutations at different loci that have accumulated in these populations, we reasoned that hybridization among independently evolved populations might restore visual function. Here we demonstrate restoration of vision in cavefish Figure 1. Map of NorthEastern Mexico indicating locations of the cave populations studied. Molino and Pachón are 53 km distant and located in different drainages. Pachón and Tinaja are over 60 km distant and also in different drainages, while the Tinaja and Curva caves are only 12 km distant and in the same drainage.
whose immediate ancestors were blind and whose separate lineages may not have been exposed to light for the last one million years. We generated numerous F1 and F2 hybrid crosses among cave populations to test whether hybrids could see, and to elucidate the underlying genetics. Purebred cave and surface fish served as controls. We also created compound hybrids by crossing F1 surface/caveA hybrids with F1 surface/caveB hybrids. Eye regression progresses with age [7], so we studied fry (9 to 40 days old), to have the best chance of detecting vision. We measured body length and eye size and tested for vision using the optokinetic response: the reflexive following of moving stripes by the subject’s eyes [9]. Purebred cavefish from Molino, Pachón and Tinaja caves were tested for their optokinetic response (Supplemental data) and/or evidence of a dorsal light reflex, visual orientation to food items or response to a looming dark object. All cavefish were blind, consistent with the observation of serious defects in both lens and retinal structure during ‘Stage III’ of eye development [7]. Quantitative trait loci (QTL) studies identified at least twelve unlinked eye loci in Pachón cavefish [2]. For purposes of discussion only, we take this number to be typical of